Skip to main content

Review of Current Evidence on the Impact of Environmental Chemicals on Gestational Diabetes Mellitus

Abstract

Pregnancy is a naturally insulin-resistant state and may be an important window of susceptibility in determining a woman’s lifetime risk of type 2 diabetes. Exposures to environmental chemicals that act as endocrine active compounds may mimic or disrupt hormones that regulate insulin action or maintain glucose homeostasis. In this commentary, we present the animal evidence that explains the biological plausibility for an association between environmental chemicals and gestational diabetes mellitus (GDM). We review the current epidemiological evidence examining the associations between GDM and bisphenol A, phthalates, air pollution, and toxic metals including arsenic and cadmium. We briefly discuss the strengths and limitations of the current evidence and offer recommendations for future studies that attempt to assess the impact environmental chemical exposure has on GDM. Lastly, we discuss the health implications for women that experience GDM during pregnancy and the importance for examining how environmental chemicals may play a role in the etiology of GDM.

This is a preview of subscription content, access via your institution.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. 1.

    IDF diabetes atlas, Sixth Edition. International Diabetes Federation; 2013.

  2. 2.

    Ferrara A. Increasing prevalence of gestational diabetes mellitus: a public health perspective. Diabetes Care. 2007;30 Suppl 2:S141–6.

    Article  PubMed  Google Scholar 

  3. 3.

    Williams D. Pregnancy: a stress test for life. Curr Opin Obstet Gynecol. 2003;15(6):465–71.

    Article  PubMed  Google Scholar 

  4. 4.

    Torgersen KL, Curran CA. A systematic approach to the physiologic adaptations of pregnancy. Crit Care Nurs Q. 2006;29(1):2–19.

    Article  PubMed  Google Scholar 

  5. 5.

    Durnwald C. Gestational diabetes: linking epidemiology, excessive gestational weight gain, adverse pregnancy outcomes, and future metabolic syndrome. Semin Perinatol. 2015;39(4):254–8.

    Article  PubMed  Google Scholar 

  6. 6.

    O’Sullivan JB. Diabetes mellitus after GDM. Diabetes. 1991;40 Suppl 2:131–5.

    Article  PubMed  Google Scholar 

  7. 7.

    Yogev Y, Catalano PM. Pregnancy and obesity. Obstet Gynecol Clin N Am. 2009;36(2):285–300. viii.

    Article  Google Scholar 

  8. 8.

    Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev. 2007;87(3):905–31.

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Mauvais-Jarvis F, Clegg DJ, Hevener AL. The role of estrogens in control of energy balance and glucose homeostasis. Endocr Rev. 2013;34(3):309–38.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Ropero AB, Alonso-Magdalena P, Quesada I, Nadal A. The role of estrogen receptors in the control of energy and glucose homeostasis. Steroids. 2008;73(9–10):874–9.

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Alonso-Magdalena P, Ropero AB, Soriano S, Garcia-Arevalo M, Ripoll C, Fuentes E, et al. Bisphenol-A acts as a potent estrogen via non-classical estrogen triggered pathways. Mol Cell Endocrinol. 2012;355(2):201–7.

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Welshons WV, Nagel SC, Vom Saal FS. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology. 2006;147(6 Suppl):S56–69.

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Batista TM, Alonso-Magdalena P, Vieira E, Amaral ME, Cederroth CR, Nef S, et al. Short-term treatment with bisphenol-A leads to metabolic abnormalities in adult male mice. PLoS One. 2012;7(3):e33814.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A. The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance. Environ Health Perspect. 2006;114(1):106–12.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Martinelli MI, Mocchiutti NO, Bernal CA. Dietary di (2-ethylhexyl) phthalate-impaired glucose metabolism in experimental animals. Hum Exp Toxicol. 2006;25(9):531–8.

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Gayathri NS, Dhanya CR, Indu AR, Kurup PA. Changes in some hormones by low doses of di (2-ethyl hexyl) phthalate (DEHP), a commonly used plasticizer in PVC blood storage bags & medical tubing. Indian J Med Res. 2004;119(4):139–44.

    CAS  PubMed  Google Scholar 

  17. 17.

    Gonzalez C, Alonso A, Fernandez R, Patterson AM. Regulation of insulin receptor substrate-1 in the liver, skeletal muscle and adipose tissue of rats throughout pregnancy. Gynecol Endocrinol. 2003;17(3):187–97.

    CAS  PubMed  Google Scholar 

  18. 18.

    Gonzalez CG, Alonso A, Balbin M, Diaz F, Fernandez S, Patterson AM. Effects of pregnancy on insulin receptor in liver, skeletal muscle and adipose tissue of rats. Gynecol Endocrinol. 2002;16(3):193–205.

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Alonso-Magdalena P, Vieira E, Soriano S, Menes L, Burks D, Quesada I, et al. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect. 2010;118(9):1243–50.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Patel HV, Kalia K. Role of hepatic and pancreatic oxidative stress in arsenic induced diabetic condition in Wistar rats. J Environ Biol. 2013;34(2):231–6.

    PubMed  Google Scholar 

  21. 21.

    Liu S, Guo X, Wu B, Yu H, Zhang X, Li M. Arsenic induces diabetic effects through beta-cell dysfunction and increased gluconeogenesis in mice. Sci Rep. 2014;4:6894.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Palacios J, Roman D, Cifuentes F. Exposure to low level of arsenic and lead in drinking water from Antofagasta city induces gender differences in glucose homeostasis in rats. Biol Trace Elem Res. 2012;148(2):224–31.

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Han JC, Park SY, Hah BG, Choi GH, Kim YK, Kwon TH, et al. Cadmium induces impaired glucose tolerance in rat by down-regulating GLUT4 expression in adipocytes. Arch Biochem Biophys. 2003;413(2):213–20.

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Trevino S, Waalkes MP, Flores Hernandez JA, Leon-Chavez BA, Aguilar-Alonso P, Brambila E. Chronic cadmium exposure in rats produces pancreatic impairment and insulin resistance in multiple peripheral tissues. Arch Biochem Biophys. 2015;583:27–35.

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Edwards JR, Prozialeck WC. Cadmium, diabetes and chronic kidney disease. Toxicol Appl Pharmacol. 2009;238(3):289–93.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Chang KC, Hsu CC, Liu SH, Su CC, Yen CC, Lee MJ, et al. Cadmium induces apoptosis in pancreatic beta-cells through a mitochondria-dependent pathway: the role of oxidative stress-mediated c-Jun N-terminal kinase activation. PLoS One. 2013;8(2):e54374.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    El MM, Raja MR, Zhang X, MacRenaris KW, Bhatt S, Chen X, et al. Accumulation of cadmium in insulin-producing beta cells. Islets. 2012;4(6):405–16.

    Article  Google Scholar 

  28. 28.

    Hill DS, Wlodarczyk BJ, Mitchell LE, Finnell RH. Arsenate-induced maternal glucose intolerance and neural tube defects in a mouse model. Toxicol Appl Pharmacol. 2009;239(1):29–36.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Yoruk M, Kanter M, Meral I, Agaoglu Z. Localization of glycogen in the placenta and fetal and maternal livers of cadmium-exposed diabetic pregnant rats. Biol Trace Elem Res. 2003;96(1–3):217–26.

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Kanter M, Yoruk M, Koc A, Meral I, Karaca T. Effects of cadmium exposure on morphological aspects of pancreas, weights of fetus and placenta in streptozotocin-induced diabetic pregnant rats. Biol Trace Elem Res. 2003;93(1–3):189–200.

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Zeng MS, Li X, Liu Y, Zhao H, Zhou JC, Li K, et al. A high-selenium diet induces insulin resistance in gestating rats and their offspring. Free Radic Biol Med. 2012;52(8):1335–42.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Ruzzin J, Petersen R, Meugnier E, Madsen L, Lock EJ, Lillefosse H, et al. Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ Health Perspect. 2010;118(4):465–71.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Ibrahim MM, Fjaere E, Lock EJ, Naville D, Amlund H, Meugnier E, et al. Chronic consumption of farmed salmon containing persistent organic pollutants causes insulin resistance and obesity in mice. PLoS One. 2011;6(9):e25170.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Mailloux R, Fu A, Florian M, Petrov I, Chen Q, Coughlan MC, et al. A Northern contaminant mixture impairs pancreas function in obese and lean JCR rats and inhibits insulin secretion in MIN6 cells. Toxicology. 2015;334:81–93.

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Nash JT, Szabo DT, Carey GB. Polybrominated diphenyl ethers alter hepatic phosphoenolpyruvate carboxykinase enzyme kinetics in male Wistar rats: implications for lipid and glucose metabolism. J Toxicol Environ Health A. 2013;76(2):142–56.

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Yanagisawa R, Koike E, Win-Shwe TT, Yamamoto M, Takano H. Impaired lipid and glucose homeostasis in hexabromocyclododecane-exposed mice fed a high-fat diet. Environ Health Perspect. 2014;122(3):277–83.

    PubMed  PubMed Central  Google Scholar 

  37. 37.

    Lasram MM, Dhouib IB, Bouzid K, Lamine AJ, Annabi A, Belhadjhmida N, et al. Association of inflammatory response and oxidative injury in the pathogenesis of liver steatosis and insulin resistance following subchronic exposure to malathion in rats. Environ Toxicol Pharmacol. 2014;38(2):542–53.

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Pakzad M, Fouladdel S, Nili-Ahmadabadi A, Pourkhalili N, Baeeri M, Azizi E, et al. Sublethal exposures of diazinon alters glucose homostasis in Wistar rats: biochemical and molecular evidences of oxidative stress in adipose tissues. Pestic Biochem Physiol. 2013;105(1):57–61.

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Ishimura R, Ohsako S, Miyabara Y, Sakaue M, Kawakami T, Aoki Y, et al. Increased glycogen content and glucose transporter 3 mRNA level in the placenta of Holtzman rats after exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol. 2002;178(3):161–71.

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Rosen MB, Lee JS, Ren H, Vallanat B, Liu J, Waalkes MP, et al. Toxicogenomic dissection of the perfluorooctanoic acid transcript profile in mouse liver: evidence for the involvement of nuclear receptors PPAR alpha and CAR. Toxicol Sci. 2008;103(1):46–56.

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Rosen MB, Abbott BD, Wolf DC, Corton JC, Wood CR, Schmid JE, et al. Gene profiling in the livers of wild-type and PPARalpha-null mice exposed to perfluorooctanoic acid. Toxicol Pathol. 2008;36(4):592–607.

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Desvergne B, Feige JN, Casals-Casas C. PPAR-mediated activity of phthalates: a link to the obesity epidemic? Mol Cell Endocrinol. 2009;304(1–2):43–8.

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Wan HT, Zhao YG, Leung PY, Wong CK. Perinatal exposure to perfluorooctane sulfonate affects glucose metabolism in adult offspring. PLoS One. 2014;9(1):e87137.

    Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Kim J, Kang EJ, Park MN, Kim JE, Kim SC, Jeung EB, et al. The adverse effect of 4-tert-octylphenol on fat metabolism in pregnant rats via regulation of lipogenic proteins. Environ Toxicol Pharmacol. 2015;40(1):284–91.

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Butenhoff JL, Ehresman DJ, Chang SC, Parker GA, Stump DG. Gestational and lactational exposure to potassium perfluorooctanesulfonate (K + PFOS) in rats: developmental neurotoxicity. Reprod Toxicol. 2009;27(3–4):319–30.

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Tada Y, Fujitani T, Yano N, Takahashi H, Yuzawa K, Ando H, et al. Effects of tetrabromobisphenol A, brominated flame retardant, in ICR mice after prenatal and postnatal exposure. Food Chem Toxicol. 2006;44(8):1408–13.

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Daruich J, Zirulnik F, Gimenez MS. Effect of the herbicide glyphosate on enzymatic activity in pregnant rats and their fetuses. Environ Res. 2001;85(3):226–31.

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Beuret CJ, Zirulnik F, Gimenez MS. Effect of the herbicide glyphosate on liver lipoperoxidation in pregnant rats and their fetuses. Reprod Toxicol. 2005;19(4):501–4.

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Xu X, Liu C, Xu Z, Tzan K, Zhong M, Wang A, et al. Long-term exposure to ambient fine particulate pollution induces insulin resistance and mitochondrial alteration in adipose tissue. Toxicol Sci. 2011;124(1):88–98.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Liu C, Xu X, Bai Y, Wang TY, Rao X, Wang A, et al. Air pollution-mediated susceptibility to inflammation and insulin resistance: influence of CCR2 pathways in mice. Environ Health Perspect. 2014;122(1):17–26.

    PubMed  PubMed Central  Google Scholar 

  51. 51.

    Zheng Z, Xu X, Zhang X, Wang A, Zhang C, Huttemann M, et al. Exposure to ambient particulate matter induces a NASH-like phenotype and impairs hepatic glucose metabolism in an animal model. J Hepatol. 2013;58(1):148–54.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Bass V, Gordon CJ, Jarema KA, MacPhail RC, Cascio WE, Phillips PM, et al. Ozone induces glucose intolerance and systemic metabolic effects in young and aged brown Norway rats. Toxicol Appl Pharmacol. 2013;273(3):551–60.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Malcolm J. Through the looking glass: gestational diabetes as a predictor of maternal and offspring long-term health. Diabetes Metab Res Rev. 2012;28(4):307–11.

    Article  PubMed  Google Scholar 

  54. 54.

    Buchanan TA, Xiang AH, Page KA. Gestational diabetes mellitus: risks and management during and after pregnancy. Nat Rev Endocrinol. 2012;8(11):639–49.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. 55.•

    Alonso-Magdalena P, Garcia-Arevalo M, Quesada I, Nadal A. Bisphenol-A treatment during pregnancy in mice: a new window of susceptibility for the development of diabetes in mothers later in life. Endocrinology. 2015;156(5):1659–70. This paper is notable because it provides animal evidence suggesting long-time health risks to mothers experiencing gestational diabetes mellitus.

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Alonso-Magdalena P, Quesada I, Nadal A. Prenatal exposure to BPA and offspring outcomes: the diabesogenic behavior of BPA. Dose Response. 2015;13(2):1559325815590395.

    Article  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Song Y, Chou EL, Baecker A, You NY, Song Y, Sun Q, et al. Endocrine-disrupting chemicals, risk of type 2 diabetes, and diabetes-related metabolic traits: a systematic review and meta-analysis. J Diabetes. 2015. doi:10.1111/1753-0407.12325.

    PubMed  Google Scholar 

  58. 58.

    Robledo C, Peck JD, Stoner JA, Carabin H, Cowan L, Koch HM, et al. Is bisphenol-A exposure during pregnancy associated with blood glucose levels or diagnosis of gestational diabetes? J Toxicol Environ Health A. 2013;76(14):865–73.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. 59.•

    Shapiro GD, Dodds L, Arbuckle TE, Ashley-Martin J, Fraser W, Fisher M, et al. Exposure to phthalates, bisphenol A and metals in pregnancy and the association with impaired glucose tolerance and gestational diabetes mellitus: the MIREC study. Environ Int. 2015;83:63–71. In a notable longitudinal Canadian birth cohort, researchers demonstrate association between metals and gestational diabetes. Associations between bisphenol-A and phthalates were not observed.

    CAS  Article  PubMed  Google Scholar 

  60. 60.

    Mahalingaiah S, Meeker JD, Pearson KR, Calafat AM, Ye X, Petrozza J, et al. Temporal variability and predictors of urinary bisphenol A concentrations in men and women. Environ Health Perspect. 2008;116(2):173–8.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Braun JM, Kalkbrenner AE, Calafat AM, Bernert JT, Ye X, Silva MJ, et al. Variability and predictors of urinary bisphenol A concentrations during pregnancy. Environ Health Perspect. 2011;119(1):131–7.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Fisher M, Arbuckle TE, Mallick R, LeBlanc A, Hauser R, Feeley M, et al. Bisphenol A and phthalate metabolite urinary concentrations: daily and across pregnancy variability. J Expo Sci Environ Epidemiol. 2015;25(3):231–9.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Robledo CA, Peck JD, Stoner J, Calafat AM, Carabin H, Cowan L, et al. Urinary phthalate metabolite concentrations and blood glucose levels during pregnancy. Int J Hyg Environ Health. 2015;218(3):324–30.

    CAS  Article  PubMed  Google Scholar 

  64. 64.

    Svensson K, Hernandez-Ramirez RU, Burguete-Garcia A, Cebrian ME, Calafat AM, Needham LL, et al. Phthalate exposure associated with self-reported diabetes among Mexican women. Environ Res. 2011;111(6):792–6.

    CAS  Article  PubMed  Google Scholar 

  65. 65.

    Casas L, Fernandez MF, Llop S, Guxens M, Ballester F, Olea N, et al. Urinary concentrations of phthalates and phenols in a population of Spanish pregnant women and children. Environ Int. 2011;37(5):858–66.

    CAS  Article  PubMed  Google Scholar 

  66. 66.

    Lind PM, Zethelius B, Lind L. Circulating levels of phthalate metabolites are associated with prevalent diabetes in the elderly. Diabetes Care. 2012;35(7):1519–24.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Sun Q, Cornelis MC, Townsend MK, Tobias DK, Eliassen AH, Franke AA, et al. Association of urinary concentrations of bisphenol A and phthalate metabolites with risk of type 2 diabetes: a prospective investigation in the nurses’ health study (NHS) and NHSII cohorts. Environ Health Perspect. 2014;122(6):616–23.

    PubMed  PubMed Central  Google Scholar 

  68. 68.

    Braun JM, Smith KW, Williams PL, Calafat AM, Berry K, Ehrlich S, et al. Variability of urinary phthalate metabolite and bisphenol A concentrations before and during pregnancy. Environ Health Perspect. 2012;120(5):739–45.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Hoppin JA, Brock JW, Davis BJ, Baird DD. Reproducibility of urinary phthalate metabolites in first morning urine samples. Environ Health Perspect. 2002;110(5):515–8.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Eze IC, Hemkens LG, Bucher HC, Hoffmann B, Schindler C, Kunzli N, et al. Association between ambient air pollution and diabetes mellitus in Europe and North America: systematic review and meta-analysis. Environ Health Perspect. 2015;123(5):381–9.

    PubMed  PubMed Central  Google Scholar 

  71. 71.

    Fleisch AF, Gold DR, Rifas-Shiman SL, Koutrakis P, Schwartz JD, Kloog I, et al. Air pollution exposure and abnormal glucose tolerance during pregnancy: the project viva cohort. Environ Health Perspect. 2014;122(4):378–83.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72.•

    Robledo CA, Mendola P, Yeung E, Mannisto T, Sundaram R, Liu D, et al. Preconception and early pregnancy air pollution exposures and risk of gestational diabetes mellitus. Environ Res. 2015;137:316–22. This study is notable because it comprehensively evaluates the association between exposure to criteria air pollutants and particulate matter with the risk of gestational diabetes. It also provides evidence to suggest that the preconception period and the first few weeks of pregnancy may be critical windows of susceptibility for gestational diabetes.

    CAS  Article  PubMed  Google Scholar 

  73. 73.•

    Malmqvist E, Jakobsson K, Tinnerberg H, Rignell-Hydbom A, Rylander L. Gestational diabetes and preeclampsia in association with air pollution at levels below current air quality guidelines. Environ Health Perspect. 2013;121(4):488–93. This was the first epidemiological study to demonstrate an association between traffic-related air pollution and gestational diabetes.

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Hu H, Ha S, Henderson BH, Warner TD, Roth J, Kan H, et al. Association of atmospheric particulate matter and ozone with gestational diabetes mellitus. Environ Health Perspect. 2015;123(9):853–9.

    PubMed  PubMed Central  Google Scholar 

  75. 75.

    Yorifuji T, Naruse H, Kashima S, Murakoshi T, Doi H. Residential proximity to major roads and obstetrical complications. Sci Total Environ. 2015;508:188–92.

    CAS  Article  PubMed  Google Scholar 

  76. 76.

    Tseng CH. The potential biological mechanisms of arsenic-induced diabetes mellitus. Toxicol Appl Pharmacol. 2004;197(2):67–83.

    CAS  Article  PubMed  Google Scholar 

  77. 77.

    Ettinger AS, Zota AR, Amarasiriwardena CJ, Hopkins MR, Schwartz J, Hu H, et al. Maternal arsenic exposure and impaired glucose tolerance during pregnancy. Environ Health Perspect. 2009;117(7):1059–64.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Peng S, Liu L, Zhang X, Heinrich J, Zhang J, Schramm KW, et al. A nested case-control study indicating heavy metal residues in meconium associate with maternal gestational diabetes mellitus risk. Environ Health. 2015;14:19.

    Article  PubMed  PubMed Central  Google Scholar 

  79. 79.

    Roverso M, Berte C, Di Marco V, Lapolla A, Badocco D, Pastore P, et al. The metallome of the human placenta in gestational diabetes mellitus. Metallomics. 2015;7(7):1146–54.

    CAS  Article  PubMed  Google Scholar 

  80. 80.

    Schwartz GG, Il’yasova D, Ivanova A. Urinary cadmium, impaired fasting glucose, and diabetes in the NHANES III. Diabetes Care. 2003;26(2):468–70.

    CAS  Article  PubMed  Google Scholar 

  81. 81.•

    Romano ME, Enquobahrie DA, Simpson CD, Checkoway H, Williams MA. A case-cohort study of cadmium body burden and gestational diabetes mellitus in American women. Environ Health Perspect. 2015;123(10):993–8. This is the first epidemiological study to report an association between cadmium and gestational diabetes.

    PubMed  PubMed Central  Google Scholar 

  82. 82.

    Needham LL, Grandjean P, Heinzow B, Jorgensen PJ, Nielsen F, Patterson Jr DG, et al. Partition of environmental chemicals between maternal and fetal blood and tissues. Environ Sci Technol. 2011;45(3):1121–6.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Adams SV, Newcomb PA. Cadmium blood and urine concentrations as measures of exposure: NHANES 1999–2010. J Expo Sci Environ Epidemiol. 2014;24(2):163–70.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  84. 84.

    Carlin DJ, Rider CV, Woychik R, Birnbaum LS. Unraveling the health effects of environmental mixtures: an NIEHS priority. Environ Health Perspect. 2013;121(1):A6–8.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Candace A. Robledo.

Ethics declarations

Conflict of Interest

C. Robledo, M. E. Romano, and P. Alonso-Magdalena declare no conflict of interest.

Human and Animal Rights and Informed Consent

All animal studies by P. Alonso-Magdalena and human studies by C. Robledo and M. Romano were performed after approval by the appropriate institutional review boards. When required, informed consent was obtained from all participants.

Additional information

This article is part of the Topical Collection on Reproductive and Perinatal Epidemiology

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Robledo, C.A., Romano, M.E. & Alonso-Magdalena, P. Review of Current Evidence on the Impact of Environmental Chemicals on Gestational Diabetes Mellitus. Curr Epidemiol Rep 3, 51–62 (2016). https://doi.org/10.1007/s40471-016-0070-z

Download citation

Keywords

  • Gestational diabetes
  • Environmental chemicals
  • Bisphenol A
  • Air pollution
  • Phthalates
  • Metals