Sociodemographic and dietary predictors of maternal and placental mycoestrogen concentrations in a US pregnancy cohort.

IF 4.1 3区 医学 Q2 ENVIRONMENTAL SCIENCES Journal of Exposure Science and Environmental Epidemiology Pub Date : 2024-10-04 DOI:10.1038/s41370-024-00722-6
Carolyn W Kinkade, Anita Brinker, Brian Buckley, Olivia Waysack, I Diana Fernandez, Amber Kautz, Ying Meng, Huishan Shi, Jessica Brunner, Pamela Ohman-Strickland, Susan W Groth, Thomas G O'Connor, Lauren M Aleksunes, Emily S Barrett, Zorimar Rivera-Núñez
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Abstract

Background: Zearalenone (ZEN) is a mycotoxin contaminating grains and processed foods. ZEN alters nuclear estrogen receptor α/β signaling earning its designation as a mycoestrogen. Experimental evidence demonstrates that mycoestrogen exposure during pregnancy is associated with altered maternal sex steroid hormones, changes in placental size, and decreases in fetal weight and length. While mycoestrogens have been detected in human biospecimens worldwide, exposure assessment of ZEN in US populations, particularly during pregnancy, is lacking.

Objective: To characterize urinary and placental concentrations of ZEN and its metabolites in healthy US pregnant people and examine demographic, perinatal, and dietary predictors of exposure.

Methods: Urine samples were collected in each trimester from pregnant participants in the UPSIDE study and placenta samples were collected at delivery (Rochester, NY, n = 317). We used high performance liquid chromatography and high-resolution tandem mass spectrometry to measure total urinary (ng/ml) and placental mycoestrogens (ng/g). Using linear regression and linear mixed effect models, we examined associations between mycoestrogen concentrations and demographic, perinatal, and dietary factors (Healthy Eating Index [HEI], ultra-processed food [UPF] consumption).

Results: Mycoestrogens were detected in 97% of urines (median 0.323 ng/ml) and 84% of placentas (median 0.012 ng/g). Stability of urinary mycoestrogens across pregnancy was low (ICC: 0.16-0.22) and did not correlate with placental levels. In adjusted models, parity (multiparous) and pre-pregnancy BMI (higher) predicted higher urinary concentrations. Birth season (fall) corresponded with higher placental mycoestrogens. Dietary analyses indicated that higher HEI (healthier diets) predicted lower exposure (e.g., Σmycoestrogens %∆ -2.03; 95%CI -3.23, -0.81) and higher percent calories from UPF predicted higher exposure (e.g., Σmycoestrogens %∆ 1.26; 95%CI 0.29, 2.24).

Impact: The mycotoxin, zearalenone (ZEN), has been linked to adverse health and reproductive impacts in animal models and livestock. Despite evidence of widespread human exposure, relatively little is known about predictors of exposure. In a pregnant population, we observed that maternal ZEN concentrations varied by maternal pre-pregnancy BMI and parity. Consumption of ultra-processed foods, added sugars, and refined grains were linked to higher ZEN concentrations while healthier diets were associated with lower levels. Our research suggests disparities in exposure that are likely due to diet. Further research is needed to understand the impacts of ZEN on maternal and offspring health.

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美国妊娠队列中母体和胎盘雌激素浓度的社会人口和饮食预测因素。
背景:玉米赤霉烯酮(ZEN)是一种污染谷物和加工食品的霉菌毒素。玉米赤霉烯酮会改变核雌激素受体 α/β 信号传导,因此被称为霉变雌激素。实验证据表明,怀孕期间接触霉变雌激素与母体性类固醇激素的改变、胎盘大小的变化以及胎儿体重和身长的减少有关。虽然在世界各地的人体生物样本中都检测到了肌醇雌激素,但在美国人群中,尤其是在怀孕期间,缺乏对 ZEN 暴露的评估:目的:确定美国健康孕妇尿液和胎盘中 ZEN 及其代谢物浓度的特征,并研究人口、围产期和饮食方面的暴露预测因素:方法: 在 UPSIDE 研究的每个孕期收集孕妇的尿液样本,并在分娩时收集胎盘样本(纽约州罗切斯特,n = 317)。我们使用高效液相色谱法和高分辨率串联质谱法测量尿液中的总雌激素(纳克/毫升)和胎盘中的总雌激素(纳克/克)。利用线性回归和线性混合效应模型,我们研究了霉菌雌激素浓度与人口统计学、围产期和饮食因素(健康饮食指数[HEI]、超加工食品[UPF]消费量)之间的关系:结果:97%的尿液(中位数为 0.323 纳克/毫升)和 84%的胎盘(中位数为 0.012 纳克/克)中检测到了霉酚雌酮。整个孕期尿液中霉菌雌激素的稳定性较低(ICC:0.16-0.22),且与胎盘中的含量不相关。在调整模型中,胎次(多胎)和孕前体重指数(较高)预示着尿液中的浓度较高。出生季节(秋季)与胎盘中较高的肌醇雌激素相对应。膳食分析表明,较高的 HEI(较健康的膳食)预示着较低的暴露量(例如,Σ 肌醇雌激素%∆ -2.03;95%CI -3.23,-0.81),而较高的 UPF 热量百分比预示着较高的暴露量(例如,Σ 肌醇雌激素%∆ 1.26;95%CI 0.29,2.24):霉菌毒素玉米赤霉烯酮(ZEN)与动物模型和牲畜的不良健康和生殖影响有关。尽管有证据表明人类广泛接触玉米赤霉烯酮,但对其接触的预测因素却知之甚少。在一个孕妇群体中,我们观察到,孕产妇的玉米赤霉烯酮浓度因孕产妇孕前体重指数(BMI)和胎次而异。食用超加工食品、添加糖和精制谷物与较高的 ZEN 浓度有关,而较健康的饮食则与较低的 ZEN 浓度有关。我们的研究表明,膳食很可能导致膳食暴露的差异。要了解 ZEN 对母体和后代健康的影响,还需要进一步的研究。
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来源期刊
CiteScore
8.90
自引率
6.70%
发文量
93
审稿时长
3 months
期刊介绍: Journal of Exposure Science and Environmental Epidemiology (JESEE) aims to be the premier and authoritative source of information on advances in exposure science for professionals in a wide range of environmental and public health disciplines. JESEE publishes original peer-reviewed research presenting significant advances in exposure science and exposure analysis, including development and application of the latest technologies for measuring exposures, and innovative computational approaches for translating novel data streams to characterize and predict exposures. The types of papers published in the research section of JESEE are original research articles, translation studies, and correspondence. Reported results should further understanding of the relationship between environmental exposure and human health, describe evaluated novel exposure science tools, or demonstrate potential of exposure science to enable decisions and actions that promote and protect human health.
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