Perinatal urinary benzophenone-3 concentrations and glucose levels among women from a fertility clinic
Tóm tắt
Subfertile women have higher risk of glucose intolerance during pregnancy. Studies suggest associations between several endocrine disrupting chemicals (EDCs) and pregnancy glucose levels. However, the association between benzophenone-3 (BP-3), an EDC widely found in sunscreen, and pregnancy glucose levels remains unclear. We aimed to assess the association between perinatal exposures to BP-3 and pregnancy glucose levels in subfertile women. We evaluated 217 women from a prospective cohort based at a fertility clinic who had urinary BP-3 concentrations measured during 3-month preconception, first and/or second trimesters, and blood glucose measured at glucose load tests (GLTs) during late pregnancy. Multivariable linear and logistic regression models were used to assess associations between time-specific BP-3 in quartiles (Q1 – Q4) and mean glucose levels, as well as odds of abnormal GLT (glucose level ≥ 140 mg/dL), adjusting for potential confounders. Effect modification was assessed by age, season, BMI, infertility diagnosis, sex of fetus (es) and physical activity. Women with higher first trimester BP-3 concentrations had lower mean glucose levels [mean glucose (95% CI) for Q4 vs Q1 = 103.4 (95.0, 112.5) vs. 114.6 (105.8, 124.2) mg/dL]. Women with higher second trimester BP-3 concentrations had lower odds of abnormal GLT [OR (95% CI) for Q3 vs. Q1 = 0.12 (0.01, 0.94)]. The associations between BP-3 and glucose levels were modified by several factors: women with female-factor infertility, urine collected during summer, older age, lower BMI, or carried female fetus (es) had the strongest inverse associations between BP-3 and glucose levels, while no associations were observed in the remaining subgroups. Time-specific inverse associations between BP-3 and pregnancy glucose levels existed in subfertile women, and especially among certain subgroups of this high-risk-population.
Tài liệu tham khảo
Casagrande SS, Linder B, Cowie CC. Prevalence of gestational diabetes and subsequent type 2 diabetes among U.S. women. Diabetes Res Clin Pract. 2018;141:200–8.
Ashrafi M, Gosili R, Hosseini R, Arabipoor A, Ahmadi J, Chehrazi M. Risk of gestational diabetes mellitus in patients undergoing assisted reproductive techniques. Eur J Obstet Gynecol Reprod Biol. 2014;176:149–52.
Holst S, Kjær SK, Jørgensen ME, Damm P, Jensen A. Fertility problems and risk of gestational diabetes mellitus: a nationwide cohort study. Fertil Steril. 2016;106:427–34.
Thoma ME, McLain AC, Louis JF, King RB, Trumble AC, Sundaram R, Louis GM. Prevalence of infertility in the United States as estimated by the current duration approach and a traditional constructed approach. Fertil Steril. 2013;99:1324–31.
HAPO Study Cooperative Research Group. Hyperglycemia and adverse pregnancy outcomes. N Engl J Med. 2008;358:1991–2002.
Riskin-Mashiah S, Younes G, Damti A, Auslender R. First-trimester fasting hyperglycemia and adverse pregnancy outcomes. Diabetes Care. 2009;32:1639–43.
Zhang C, Rawal S, Chong YS. Risk factors for gestational diabetes: is prevention possible? Diabetologia. 2016;59:1385–90.
Ehrlich S, Lambers D, Baccarelli A, Khoury J, Macaluso M, Ho SM. Endocrine disruptors: a potential risk factor for gestational diabetes mellitus. Am J Perinatol. 2016;33:1313–8.
Eslami B, Naddafi K, Rastkari N, Rashidi BH, Djazayeri A, Malekafzali H. Association between serum concentrations of persistent organic pollutants and gestational diabetes mellitus in primiparous women. Environ Res. 2016;151:706–12.
Chiu YH, Mínguez-Alarcón L, Ford JB, Keller M, Seely EW, Messerlian C, Petrozza J, Williams PL, Ye X, Calafat AM, Hauser R. Trimester-specific urinary bisphenol a concentrations and blood glucose levels among pregnant women from a fertility clinic. J Clin Endocrinol Metab. 2017;102:1350–7.
Bellavia A, Chiu YH, Brown FM, Mínguez-Alarcón L, Ford JB, Keller M, Petrozza J, Williams PL, Ye X, Calafat AM, Hauser R. Urinary concentrations of parabens mixture and pregnancy glucose levels among women from a fertility clinic. Environ Res. 2019;168:389–96.
James-Todd TM, Chiu YH, Messerlian C, Mínguez-Alarcón L, Ford JB, Keller M, Petrozza J, Williams PL, Ye X, Calafat AM, Hauser R. Trimester-specific phthalate concentrations and glucose levels among women from a fertility clinic. Environ Health. 2018;17:55.
Tchernof A. Sex differences in energy balance, body composition, and body fat distribution. In: Tsatsoulis WJ, Brown FM, editors. Diabetes in women: Pathphysiology and therapy. New York: US: Humana press/springer science+business media; 2009.
Han C, Lim YH, Hong YC. Ten-year trends in urinary concentrations of triclosan and benzophenone-3 in the general U.S. population from 2003 to 2012. Environ Pollut. 2016;208:803–10.
Mortensen ME, Calafat AM, Ye X, Wong LY, Wright DJ, Pirkle JL, Merrill LS, Moye J. Urinary concentrations of environmental phenols in pregnant women in a pilot study of the National Children’s study. Environ Res. 2014;129:32–8.
Calafat AM, Wong LY, Ye X, Reidy JA, Needham LL. Concentrations of the sunscreen agent benzophenone-3 in residents of the United States: National Health and nutrition examination survey 2003-2004. Environ Health Perspect. 2008;116:893–7.
Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A. The estrogenic effect of bisphenol a disrupts pancreatic β-cell function in vivo and induces insulin resistance. Environ Health Perspect. 2006;114:106–12.
Holland N, Huen K, Tran V, Street K, Nguyen B, Bradman A, Eskenazi B. Urinary phthalate metabolites and biomarkers of oxidative stress in a Mexican-American cohort: variability in early and late pregnancy. Toxics. 2016;4:7.
Artacho-Cordón F, Ríos-Arrabal S, León J, Frederiksen H, Sáenz JM, Martín-Olmedo P, Fernández MF, Olea N, Arrebola JP. Adipose tissue concentrations of non-persistent environmental phenols and local redox balance in adults from southern Spain. Environ Int. 2019;133:105118.
Krause M, Frederiksen H, Sundberg K, Jørgensen FS, Jensen LN, Nørgaard P, Jørgensen C, Ertberg P, Petersen JH, Feldt-Rasmussen U, Juul A. Maternal exposure to UV filters: associations with maternal thyroid hormones, IGF-I/IGFBP3 and birth outcomes. Endocr Connect. 2018;7:334–46.
Watkins DJ, Ferguson KK, Del Toro LV, Alshawabkeh AN, Cordero JF, Meeker JD. Associations between urinary phenol and paraben concentrations and markers of oxidative stress and inflammation among pregnant women in Puerto Rico. Int J Hyg Environ Health. 2015;218:212–9.
Ferguson KK, Lan Z, Yu Y, Mukherjee B, McElrath TF, Meeker JD. Urinary concentrations of phenols in association with biomarkers of oxidative stress in pregnancy: assessment of effects independent of phthalates. Environ Int. 2019;131:104903.
Li AJ, Xue J, Lin S, Al-Malki AL, Al-Ghamdi MA, Kumosani TA, Kannan K. Urinary concentrations of environmental phenols and their association with type 2 diabetes in a population in Jeddah, Saudi Arabia. Environ Res. 2018;166:544–52.
Philippat C, Nakiwala D, Calafat AM, Botton J, De Agostini M, Heude B, Slama R. EDEN mother–child study group. Prenatal exposure to nonpersistent endocrine disruptors and behavior in boys at 3 and 5 years. Environ Health Perspect. 2017;125:097014.
Freemark M. Regulation of maternal metabolism by pituitary and placental hormones: roles in fetal development and metabolic programming. Horm Res Paediatr. 2006;65:41–9.
Messerlian C, Williams PL, Ford JB, Chavarro JE, Mínguez-Alarcón L, Dadd R, Braun JM, Gaskins AJ, Meeker JD, James-Todd T, Chiu YH. The Environment and Reproductive Health (EARTH) Study: a prospective preconception cohort. Hum Reprod Open. 2018;2018:hoy001.
Pearson MA, Lu C, Schmotzer BJ, Waller LA, Riederer AM. Evaluation of physiological measures for correcting variation in urinary output: implications for assessing environmental chemical exposure in children. J Expo Sci Environ Epidemiol. 2009;19:336.
Silva MJ, Samandar E, Preau JL Jr, Reidy JA, Needham LL, Calafat AM. Quantification of 22 phthalate metabolites in human urine. J Chromatogr B. 2007;860:106–12.
Gupta Y, Kalra B, Baruah M, Singla R, Kalra S. Updated guidelines on screening for gestational diabetes. Int J Women's Health. 2015;7:539.
Hornung RW, Reed LD. Estimation of average concentrations in the presence of nondetectable values. Appl Occup Environ Hyg. 1990;5:46–51.
Mirghani Dirar A, Doupis J. Gestational diabetes from a to Z. World J Diabetes. 2017;8:489–511.
Chiefari E, Pastore I, Puccio L, Caroleo P, Oliverio R, Vero A. P Foti D, Vero R, Brunetti a. impact of seasonality on gestational diabetes mellitus. Endocr Metab Immune Disord Drug Targets. 2017;17:246–52.
Oda E. High-sensitivity C-reactive protein, but not white blood cell count, independently predicted incident diabetes in a Japanese health screening population. Acta Diabetol. 2015;52:983–90.
Yamasaki K, Okuda H, Kikkawa H. Endocrine-mediated effects of a benzophenone related chemical, 2,3,4,4′-Tetrahydroxybenzophenone, based on uterotrophic assay, hershberger assay, and subacute oral toxicity study. J Clin Toxicol. 2012;2:129.
Burdock GA, Ford RA, Cliffs E, Manufacturers E. Safety evaluation of benzophenone. Food Chem Toxicol. 1991;29:741–50.
Kim S, Choi K. Occurrences, toxicities, and ecological risks of BP-3, a common component of organic sunscreen products: a mini-review. Environ Int. 2014;70:143–57.
Pollack AZ, Mumford SL, Krall JR, Carmichael AE, Sjaarda LA, Perkins NJ, Kannan K, Schisterman EF. Exposure to bisphenol a, chlorophenols, benzophenones, and parabens in relation to reproductive hormones in healthy women: a chemical mixture approach. Environ Int. 2018;120:137–44.
Mauvais-Jarvis F, Clegg DJ, Hevener AL. The role of estrogens in control of energy balance and glucose homeostasis. Endocr Rev. 2013;34:309–38.
Rawal S, Tsai MY, Hinkle SN, Zhu Y, Bao W, Lin Y, Panuganti P, Albert PS, Ma RC, Zhang C. A longitudinal study of thyroid markers across pregnancy and the risk of gestational diabetes. J Clin Endocrinol Metab. 2018;103:2447–56.
Lee J, Kim S, Park YJ, Moon HB, Choi K. Thyroid hormone-disrupting potentials of major benzophenones in two cell lines (GH3 and FRTL-5) and embryo-larval zebrafish. Environ Sci Technol. 2018;52:8858–65.
Aker AM, Johns L, McElrath TF, Cantonwine DE, Mukherjee B, Meeker JD. Associations between maternal phenol and paraben urinary biomarkers and maternal hormones during pregnancy: a repeated measures study. Environ Int. 2018;113:341–9.
Klieverik LP, Janssen SF, van Riel A, Foppen E, Bisschop PH, Serlie MJ, Boelen A, Ackermans MT, Sauerwein HP, Fliers E, Kalsbeek A. Thyroid hormone modulates glucose production via a sympathetic pathway from the hypothalamic paraventricular nucleus to the liver. Proc Natl Acad Sci. 2009;106:5966–71.
Li C, Deng X, Xie X, Liu Y, Friedmann Angeli JP, Lai L. Activation of glutathione peroxidase 4 as a novel anti-inflammatory strategy. Front Pharmacol. 2018;9:1120.
Koulajian K, Ivovic A, Ye K, Desai T, Shah A, George Fantus I, Ran Q, Giacca A. Overexpression of glutathione peroxidase 4 prevents β-cell dysfunction induced by prolonged elevation of lipids in vivo. Am J Physiol Endocrinol Metab. 2013;305(2):E254–62.
Qiu C, Sorensen TK, Luthy DA, Williams MA. A prospective study of maternal serum C-reactive protein (CRP) concentrations and risk of gestational diabetes mellitus. Paediatr Perinat Epidemiol. 2004;18:377–84.
Mínguez-Alarcón L, Chiu YH, Nassan FL, Williams PL, Petrozza J, Ford JB, Calafat AM, Hauser R, Chavarro JE. Earth Study Team. Urinary concentrations of benzophenone-3 and reproductive outcomes among women undergoing infertility treatment with assisted reproductive technologies. Sci Total Environ. 2019;678:390–8.
Bellavia A, Mínguez-Alarcón L, Ford JB, Keller M, Petrozza J, Williams PL, Hauser R, James-Todd T. EARTH study team. Association of self-reported personal care product use with blood glucose levels measured during pregnancy among women from a fertility clinic. Sci Total Environ. 2019;695:133855.
Arnold DL, Enquobahrie DA, Qiu C, Huang J, Grote N, VanderStoep A, Williams MA. Early pregnancy maternal vitamin D concentrations and risk of gestational diabetes mellitus. Paediatr Perinat Epidemiol. 2015;29:200–10.
Retnakaran R, Kramer CK, Ye C, Kew S, Hanley AJ, Connelly PW, Sermer M, Zinman B. Fetal sex and maternal risk of gestational diabetes mellitus: the impact of having a boy. Diabetes Care. 2015;38:844–51.
Jaskolka D, Retnakaran R, Zinman B, Kramer CK. Sex of the baby and risk of gestational diabetes mellitus in the mother: a systematic review and meta-analysis. Diabetologia. 2015;58:2469–75.
Mortensen ME, Caudill SP, Caldwell KL, Ward CD, Jones RL. Total and methyl mercury in whole blood measured for the first time in the US population: NHANES 2011–2012. Environ Res. 2014;134:257–64.