Contaminants and Nutrients in Seafood: Exposure and Mortality in Population at Risk

BACKGROUND: Fish and shellfish are good sources of nutrients but also accumulate environmental pollutants, such as polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane (DDE), and mercury, which have detrimental impacts on many health outcomes. Despite the declining contaminant levels in Great Lakes fish , DDE and PCBs exposures remain higher among frequent Great Lakes sports fish consumers than the general population. Asian populations in the United States have higher Hg levels compared to other racial/ethnic groups due to their higher seafood consumption. Different patterns of fish consumption habits and exposure to environmental pollutants make Great Lakes fishermen and the Asian population in the United States vulnerable to adverse health outcomes. The main objectives of this study were to investigate the correlation between intake estimation of contaminants in fish and biomarkers of contaminants in the human body among susceptible populations, and to analyze the effects of fish consumption on human health. First, we aimed to estimate the average daily intake of PCBs (ADIPCBs) from Great Lakes fish consumption and to assess the correlation between ADIPCBs and measured blood PCBs levels among Great Lakes sports fish consumers. Second, we examined the effects of fish consumption and PCB and DDE exposures on cause-specific mortality in the Great Lakes Fish Consumption Study cohort. Third, to understand the exposure patterns to methylmercury (MeHg) among Asian population in the United States, we calculated the average daily MeHg intake from different seafood species and assessed the relationship between seafood meals and Average Daily Methylmercury Intake (ADMI) with blood MeHg concentrations among the Asian and Non-Asian U.S. population. METHODS: Effects of fish consumption and PCB and DDE exposures on cause-specific mortality, and risk assessment of PCBs through sports fish consumption was conducted using the Great Lakes Fish Consumption Study (GLFCS) cohort. Correlations between ADIPCBs and log transformed serum PCBs were examined using multivariable linear regression. Mortality data for the GLFCS cohort was ascertained from the National Death Index (NDI) database from 1994 to 2015. Crude cause-specific mortality in relation to fish consumption and PCBs/DDEs was calculated and Cox proportional hazards models were applied to calculate risk of cause-specific death in relation to fish consumption and PCBs/DDEs, adjusting for covariates. Multiple imputation by chained equations (MICE) was applied to impute multivariate missing data for the full cohort. Subgroup analysis was conducted among participants with complete data on PCBs/DDEs and other risk factors. Two recent National Health and Nutrition Examination Survey (NHANES) cycles (2011/2012 and 2013/2014) were combined to assess correlations between BMeHg, TBHg, and seafood consumption among Asian and Non-Asian U.S. populations. Seafood consumption was collected using self-reported in person dietary recall interviews over the past 30 days. Multivariable linear regression of the natural log transformed BMeHg and TBHg concentrations on the log of the mean ADMI or the number of seafood meals, adjusting for covariates, was conducted. Survey design variables and sampling weights were applied to adjust for differential selection probabilities in NHANES. All statistical analyses were conducted with SAS (version 9.3; SAS Institute Inc., Cary, NC). RESULTS: Mean ADIPCBs from Great Lakes fish ranged from 0.0002 μg/kg-day for catfish and carp from Lake Michigan to 0.025 μg/kg-day for lake trout from Lake Michigan. Overall, 29.8% (152 out of 511) of captains had ADIPCBs exceeding health protective value proposed by the Task Force (0.05 ug/kg/day). Captains who mainly consumed sports fish from Lake Michigan had the highest proportion of exceeding the health protective value (46.1%), whereas, captains who mainly consumed sports fish from inland water had the lowest proportion of exceeding the health protective value (10.9%), Correlations between serum PCBs and ADIPCBs were higher among female participants than their male counterparts. Correlations between serum PCBs and ADIPCBs were also higher among Wisconsin anglers who mainly consumed fish from inland water bodies than captains who consumed sports fish from Great Lakes. A total of 3,892 subjects were followed from January 1, 1995 through December 31, 2015 and contributed 75,741 person-years at risk of death. Mean age at death was 70.4 years. During the mean of 19 years (range: 0-21 years) follow up, 710 subjects were ascertained as deceased by NDI. The leading cause of death was CVD, followed by cancer and respiratory disease. Consumption of ≥ one total fish meal per week (commercial or sports fish) was associated with a decreased all-cause mortality compared with consumption of < 1 fish meal per month, after adjusting for sex, age, income and baseline BMI. However, the association between fish consumption and all-cause mortality were only borderline statistically significant among all participants (HR=0.86; 95%CI: 0.71-1.03) and referents (HR=0.73; 95%CI: 0.52-1.04). Similarly, consumption of ≥ one total fish meals per week was statistically significant associated with 22% reduction in CVD mortality among all participants (HR=0.78; 95%CI: 0.60-0.98) and a 41% reduction among referents (HR=0.59; 95%CI: 0.37-0.94), but no statistically significant association was observed among captains (HR=0.86; 95%CI: 0.63-1.17). A statistically significant dose-related protective effect of total fish consumption against CVD mortality was observed among all participants and among referent group (P for trend: 0.04 for total cohort; 0.03 for referents). Neither captains nor referents showed statistically significant associations between total fish consumption and diabetes or cancer mortality. A statistically significant dose-related protective effect of total fish consumption against diabetes mortality was observed in full cohort (P for trend=0.02) and in referents (P for trend=0.02). This protective effect of total fish consumption against diabetes mortality was also present in captains, however, the association was not statistically significant. A non-significant trend for an inverse U-Shape relationship of GL fish consumption and cardiovascular disease (CVD) mortality was detected in the subgroup analysis, with eating >=1 GL fish meal per week associated with the lowest CVD mortality. Total fish and GL fish consumption of > 1 serving per week was inversely, but not significantly, associated with diabetes mortality, while serum PCBs and DDE levels were associated with non-significantly increased diabetes mortality. Consumption of ≥ one GL fish meal per week was associated with a significant increased diabetes mortality (HR=2.17; 95%CI: 0.91-5.21) after adjusting for covariates. Consumption of ≥ one GL fish meal per month but less than one GL fish meal per week was associated with a borderline significant increased cancer mortality (HR=1.39; 95%CI: 0.97-1.99) after adjusting for covariates. Analysis of 2011-2014 NHANES found that both Asian women of reproductive age (WORA) and Asian adults age ≥ 50 years of age had significantly higher BMeHg levels and ADMI from 30-day recall of seafood consumption than their Non-Asian counterparts. Average Daily MeHg explained 38% and 19% of the variance in blood MeHg level for Asian WORA and Asian adults age ≥ 50 years old, respectively. Correlations between ADMI and blood Hg level were stronger among Asian WORA than among Non-Asian WORA, but weaker among Asian adults age ≥ 50 years old than among Non-Asian adults age ≥ 50 years old. Sources of variation of BMeHg among Asian adults age ≥ 50 years old other than fish intake might explain the apparent moderate association of MeHg intake and blood MeHg level. CONCLUSION: Our finding of Great Lakes Fish Consumption Cohort found nearly a third of the captains had estimated daily intake of PCBs from sports fish exceeding the Task Force health protective value. Our results also suggested that average daily intake of PCBs estimated from fish consumption survey might not be an ideal proxy for serum PCBs concentration. However, without invasive biomarker assessment available, the fish consumption data might be useful to estimate the daily intake of PCBs through dietary exposure for females frequent sports fish consumers. Our full cohort analysis of GLFCS found that total fish intake was associated with a significant protective effect against CVD mortality among the entire cohort and among referent population. However, captains, who primarily consumed GL sports fish, did not experience the protective effect of fish consumption on CVD or all-cause mortality. Our analysis of the mercury exposure profile among the Asian population in the U.S. suggested that fish consumption is a key predictor of blood MeHg concentration, especially among Asian women of reproductive age. Mercury guidance and intervention among Asians in the US, particularly subgroups at higher risk of mercury exposure, is warranted due to their fish consumption behavior.