Exposure to endocrine-disrupting chemicals during pregnancy and weight at 7 years of age: A multi-pollutant approach

Environmental Health Perspectives

Volumn 123, Issue 10, 2015, Pages 1030-1037

  Agay Shay, Keren ^a,b,c   Martinez, David ^a,b,c   Valvi, Damaskini ^a,b,c   Garcia Esteban, Raquel ^a,b,c   Basagaña, Xavier ^a,b,c   Robinson, Oliver ^a,b,c   Casas, Maribel ^a,b,c   Sunyer, Jordi ^a,b,c,d   Vrijheid, Martine ^a,b,c  

^a CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^d HOSPITAL DEL MAR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA HEXACHLOROCYCLOHEXANE; ENDOCRINE DISRUPTOR; HEXACHLOROBENZENE; POLYCHLORINATED BIPHENYL DERIVATIVE; POLLUTANT;

ANTHROPOMETRY; ARTICLE; BODY WEIGHT; CARDIOMETABOLIC RISK; CLINICAL EVALUATION; DEMOGRAPHY; ENVIRONMENTAL HEALTH; FEMALE; HUMAN; MAJOR CLINICAL STUDY; OBESITY; ORGANIC POLLUTION; PREGNANCY; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PUBLIC HEALTH PROBLEM; RISK ASSESSMENT; STATISTICAL ANALYSIS; WEIGHT GAIN; ADOLESCENT; ADULT; BLOOD; BLOOD PRESSURE; BODY MASS; CHEMICALLY INDUCED; CHILD; COHORT ANALYSIS; DRUG EFFECTS; EPIDEMIOLOGY; MALE; METABOLISM; POLLUTANT; SPAIN; TOXICITY; URINE; WAIST TO HEIGHT RATIO; YOUNG ADULT;

ADOLESCENT; ADULT; BLOOD PRESSURE; BODY MASS INDEX; BODY WEIGHT; CHILD; COHORT STUDIES; ENDOCRINE DISRUPTORS; ENVIRONMENTAL POLLUTANTS; FEMALE; HUMANS; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SPAIN; WAIST-HEIGHT RATIO; YOUNG ADULT;

EID: 84940833646     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1409049     Document Type: Article

References (75)

1. Andersen CS, Fei C, Gamborg M, Nohr EA, Sørensen TI, Olsen J. 2013. Prenatal exposures to perfluorinated chemicals and anthropometry at 7 years of age. Am J Epidemiol 178(6):921-927.
2. Arif AA, Shah SM. 2007. Association between personal exposure to volatile organic compounds and asthma among US adult population. Int Arch Occup Environ Health 80(8):711-719.
3. Azur MJ, Stuart EA, Frangakis C, Leaf PJ. 2011. Multiple imputation by chained equations: what is it and how does it work? Int J Methods Psychiatr Res 20(1):40-49.
4. Baker JL, Olsen LW, Sørensen TI. 2007. Childhood bodymass index and the risk of coronary heart disease in adulthood. N Engl J Med 357(23):2329-2337.
5. Basagaña X, Barrera-Gómez J, Benet M, Antó JM, Garcia-Aymerich J. 2013. A framework for multiple imputation in cluster analysis. Am J Epidemiol 177(7):718-725; doi:10.1093/aje/kws289.
6. Billionnet C, Sherrill D, Annesi-Maesano I, GERIE Study. 2012. Estimating the health effects of exposure to multi-pollutant mixture. Ann Epidemiol 22(2):126-141; doi:10.1016/j.annepidem.2011.11.004.
7. Blanck HM, Marcus M, Rubin C, Tolbert PE, Hertzberg VS, Henderson AK, et al. 2002. Growth in girls exposed in utero and postnatally to polybrominated biphenyls and polychlorinated biphenyls. Epidemiology 13(2):205-210.
8. Braun JM, Kalkbrenner AE, Just AC, Yolton K, Calafat AM, Sjödin A, et al. 2014. Gestational exposure to endocrine-disrupting chemicals and reciprocal social, repetitive, and stereotypic behaviors in 4-and 5-year-old children: the HOME study. Environ Health Perspect 122:513-520; doi:10.1289/ ehp.1307261.
9. Brown JD. 2009. Choosing the right number of components or factors in PCA and EFA. JALT Testing Eval SIG Newsletter 13(2):19-23.
10. Casas M, Valvi D, Luque N, Ballesteros-Gomez A, Carsin A, Fernandez MF, et al. 2013. Dietary and sociodemographic determinants of bisphenol A urine concentrations in pregnant women and children. Environ Int 56:10-18; doi:10.1016/j. envint.2013.02.014.
11. Cupul-Uicab LA, Hernández-Ávila M, TerrazasMedina EA, Pennell ML, Longnecker MP. 2010. Prenatal exposure to the major DDT metabolite 1,1-dichloro-2,2-bis (p-chlorophenyl) ethylene (DDE) and growth in boys from Mexico. Environ Res 110(6):595-603.
12. de Onis M, Garza C, Onyango AW, Rolland-Cachera MF, le Comité de nutrition de la Société française de pédiatrie. 2009. WHO growth standards for infants and young children [in French]. Arch Pediatr 16:47-53.
13. de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. 2007. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 85:660-667.
14. Delvaux I, Van Cauwenberghe J, Den Hond E, Schoeters G, Govarts E, Nelen V, et al. 2014. Prenatal exposure to environmental contaminants and body composition at age 7-9 years. Environ Res 132:24-32; doi:10.1016/j.envres.2014.03.019.
15. Desai M, Esserman DA, Gammon MD, Terry MB. 2011a. The use of complete-case and multiple imputationbased analyses in molecular epidemiology studies that assess interaction effects. Epidemiol Perspect Innov 8(1):5; doi:10.1186/1742-5573-8-5.
16. Desai M, Kubo J, Esserman D, Terry MB. 2011b. The handling of missing data in molecular epidemiology studies. Cancer Epidemiol Biomarkers Prev 20(8):1571-1579.
17. Forns J, Fort M, Casas M, Cáceres A, Guxens M, Gascon M, et al. 2013. Exposure to metals during pregnancy and neuropsychological development at the age of 4 years. Neurotoxicology 40:16-22.
18. Fort M, Cosín-Tomás M, Grimalt JO, Querol X, Casas M, Sunyer J. 2014. Assessment of exposure to trace metals in a cohort of pregnant women from an urban center by urine analysis in the first and third trimesters of pregnancy. Environ Sci Pollut Res Int 21(15):9234-9241.
19. Gardner RM, Kippler M, Tofail F, Bottai M, Hamadani J, Grander M, et al. 2013. Environmental exposure to metals and children's growth to age 5 years: a prospective cohort study. Am J Epidemiol 177(12):1356-1367; doi:10.1093/aje/kws437.
20. Gascon M, Fort M, Martínez D, Carsin A, Forns J, Grimalt JO, et al. 2012. Polybrominated diphenyl ethers (PBDEs) in breast milk and neuropsychological development in infants. Environ Health Perspect 120:1760-1765; doi:10.1289/ehp.1205266.
21. Gladen BC, Klebanoff MA, Hediger ML, Katz SH, Barr DB, Davis MD, et al. 2004. Prenatal DDT exposure in relation to anthropometric and pubertal measures in adolescent males. Environ Health Perspect 112:1761-1767; doi:10.1289/ehp.7287.
22. Gladen BC, Ragan NB, Rogan WJ. 2000. Pubertal growth and development and prenatal and lactational exposure to polychlorinated biphenyls and dichlorodiphenyl dichloroethene. J Pediatr 136(4):490-496.
23. Graham JW. 2009. Missing data analysis: making it work in the real world. Annu Rev Psychol 60:549-576.
24. Grandjean P, Andersen EW, Budtz-Jørgensen E, Nielsen F, Mølbak K, Weihe P, et al. 2012. Serum vaccine antibody concentrations in children exposed to perfluorinated compounds. JAMA 307(4):391-397.
25. Grün F, Blumberg B. 2009. Endocrine disrupters as obesogens. Mol Cell Endocrinol 304(1-2):19-29.
26. Guxens M, Ballester F, Espada M, Fernández MF, Grimalt JO, Ibarluzea J, et al. 2012. Cohort profile: the INMA-INfancia y Medio Ambiente- (Environment and Childhood) Project. Int J Epidemiol 41(4):930-940; doi:10.1093/ije/dyr054.
27. Halldorsson TI, Rytter D, Haug LS, Bech BH, Danielsen I, Becher G, et al. 2012. Prenatal exposure to perfluorooctanoate and risk of overweight at 20 years of age: a prospective cohort study. Environ Health Perspect 120:668-673; doi:10.1289/ehp.1104034.
28. Han JC, Lawlor DA, Kimm SY. 2010. Childhood obesity. Lancet 375(9727):1737-1748.
29. Harley KG, Aguilar Schall R, Chevrier J, Tyler K, Aguirre H, Bradman A, et al. 2013. Prenatal and postnatal bisphenol A exposure and body mass index in childhood in the CHAMACOS cohort. Environ Health Perspect 121:514-520; doi:10.1289/ ehp.1205548.
30. Hatcher L. 1994. A Step-by-Step Approach to Using the SAS System for Factor Analysis and Structural Equation Modeling. Cary, NC:SAS Institute.
31. Heitjan DF. 2011. Incomplete data: what you don't know might hurt you. Cancer Epidemiol Biomarkers Prev 20(8):1567-1570; doi:10.1158/1055-9965.EPI-11-0505.
32. Hertz-Picciotto I, Charles MJ, James RA, Keller JA, Willman E, Teplin S. 2005. In utero polychlorinated biphenyl exposures in relation to fetal and early childhood growth. Epidemiology 16(5):648-656.
33. Holtcamp W. 2012. Obesogens: an environmental link to obesity. Environ Health Perspect 120:A62-A68; doi:10.1289/ehp.120-a62.
34. Huang JS, Lee TA, Lu MC. 2007. Prenatal programming of childhood overweight and obesity. Matern Child Health J 11(5):461-473.
35. IOM (Institute of Medicine). 2009. Weight Gain During Pregnancy: Reexamining the Guidelines (Rasmussen KM, Yaktine AL, eds). Washington, DC:National Academies Press. Available: http://www.nap. edu/openbook.php?record_id=12584&page=R1 [accessed 7 August 2014].
36. Jacobson JL, Jacobson SW, Humphrey HE. 1990. Effects of exposure to PCBs and related compounds on growth and activity in children. Neurotoxicol Teratol 12(4):319-326.
37. Kant AK. 2004. Dietary patterns and health outcomes. J Am Diet Assoc 104(4):615-635.
38. Karmaus W, Osuch JR, Eneli I, Mudd LM, Zhang J, Mikucki D, et al. 2009. Maternal levels of dichlorodiphenyl-dichloroethylene (DDE) may increase weight and body mass index in adult female offspring. Occup Environ Med 66(3):143-149; doi:10.1136/oem.2008.041921.
39. Klebanoff MA, Cole SR. 2008. Use of multiple imputation in the epidemiologic literature. Am J Epidemiol 168(4):355-357; doi:10.1093/aje/kwn071.
40. La Merrill M, Birnbaum LS. 2011. Childhood obesity and environmental chemicals. Mt Sinai J Med 78(1):22-48.
41. La Merrill M, Emond C, Kim MJ, Antignac J, Le Bizec B, Clément K, et al. 2013. Toxicological function of adipose tissue: focus on persistent organic pollutants. Environ Health Perspect 121:162-169. doi:10.1289/ehp.1205485.
42. Lamb MR, Taylor S, Liu X, Wolff MS, Borrell L, Matte TD, et al. 2006. Prenatal exposure to polychlorinated biphenyls and postnatal growth: a structural analysis. Environ Health Perspect 114:779-785; doi:10.1289/ehp.8488.
43. Lampa E, Lind L, Lind PM, Bornefalk-Hermansson A. 2014. The identification of complex interactions in epidemiology and toxicology: a simulation study of boosted regression trees. Environ Health 13:57; doi:10.1186/1476-069X-13-57.
44. Lee DH, Lee IK, Porta M, Steffes M, Jacobs D Jr. 2007. Relationship between serum concentrations of persistent organic pollutants and the prevalence of metabolic syndrome among non-diabetic adults: results from the National Health and Nutrition Examination Survey 1999-2002. Diabetologia 50(9):1841-1851.
45. Lee DH, Porta M, Jacobs DR Jr, Vandenberg LN. 2014. Chlorinated persistent organic pollutants, obesity, and type 2 diabetes. Endocr Rev 35(4):557-601.
46. Lee D, Steffes MW, Sjödin A, Jones RS, Needham LL, Jacobs DR Jr. 2010. Low dose of some persistent organic pollutants predicts type 2 diabetes: a nested case-control study. Environ Health Perspect 118:1235-1242; doi:10.1289/ehp.0901480.
47. Lenters V, Portengen L, Smit LA, Jonsson BA, Giwercman A, Rylander L, et al. 2015. Phthalates, perfluoroalkyl acids, metals and organochlorines and reproductive function: a multipollutant assessment in Greenlandic, Polish and Ukrainian men. Occup Environ Med 72(6):385-393; doi:10.1136/ oemed-2014-102264.
48. Li KH, Meng XL, Raghunathan TE, Rubin DB. 1991. Significance levels from repeated p-values with multiply-imputed data. Stat Sin 1(1):65-92.
49. Llop S, Guxens M, Murcia M, Lertxundi A, Ramon R, Riaño I, et al. 2012. Prenatal exposure to mercury and infant neurodevelopment in a multicenter cohort in Spain: study of potential modifiers. Am J Epidemiol 175(5):451-465; doi:10.1093/aje/kwr328.
50. Maisonet M, Terrell ML, McGeehin MA, Christensen KY, Holmes A, Calafat AM, et al. 2012. Maternal concentrations of polyfluoroalkyl compounds during pregnancy and fetal and postnatal growth in British girls. Environ Health Perspect 120:1432-1437; doi:10.1289/ ehp.1003096.
51. Mauderly JL, Burnett RT, Castillejos M, Özkaynak H, Samet JM, Stieb DM, et al. 2010. Is the air pollution health research community prepared to support a multipollutant air quality management framework? Inhal Toxicol 22(suppl 1):1-19.
52. Mendez MA, Garcia-Esteban R, Guxens M, Vrijheid M, Kogevinas M, Goñi F, et al. 2011. Prenatal organochlorine compound exposure, rapid weight gain, and overweight in infancy. Environ Health Perspect 119:272-278; doi:10.1289/ehp.1002169.
53. Oken E, Levitan E, Gillman M. 2008. Maternal smoking during pregnancy and child overweight: systematic review and meta-analysis. Int J Obes (Lond) 32(2):201-210.
54. Patandin S, Koopman-Esseboom C, de Ridder MA, Weisglas-Kuperus N, Sauer PJ. 1998. Effects of environmental exposure to polychlorinated biphenyls and dioxins on birth size and growth in Dutch children. Pediatr Res 44(4):538-545.
55. Patel CJ, Bhattacharya J, Butte AJ. 2010. An Environment-Wide Association Study (EWAS) on type 2 diabetes mellitus. PLoS One 5(5):e10746; doi:10.1371/journal.pone.0010746.
56. Perneger TV. 1998. What's wrong with Bonferroni adjustments. BMJ 316(7139):1236-1238.
57. Qian Z, Zhang J, Korn LR, Wei F, Chapman RS. 2004. Factor analysis of household factors: are they associated with respiratory conditions in Chinese children? Int J Epidemiol 33(3):582-588.
58. Rothman KJ. 1990. No adjustments are needed for multiple comparisons. Epidemiology 1(1):43-46.
59. Royston P, White IR. 2011. Multiple imputation by chained equations (MICE): implementation in Stata. J Stat Softw 45(4):1-20.
60. Smink A, Ribas-Fito N, Garcia R, Torrent M, Mendez MA, Grimalt JO, et al. 2008. Exposure to hexachlorobenzene during pregnancy increases the risk of overweight in children aged 6 years. Acta Paediatr 97(10):1465-1469.
61. Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, et al. 2009. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ 338:b2393; doi:10.1136/bmj.b2393.
62. Sun Z, Tao Y, Li S, Ferguson KK, Meeker JD, Park SK, et al. 2013. Statistical strategies for constructing health risk models with multiple pollutants and their interactions: possible choices and comparisons. Environ Health 12(1):85; doi:10.1186/1476-069X-12-85.
63. Tang-Péronard JL, Andersen HR, Jensen TK, Heitmann BL. 2011. Endocrine-disrupting chemicals and obesity development in humans: a review. Obes Rev 12(8):622-636.
64. Tang-Péronard JL, Heitmann BL, Andersen HR, Steuerwald U, Grandjean P, Weihe P, et al. 2014. Association between prenatal polychlorinated biphenyl exposure and obesity development at ages 5 and 7 y: a prospective cohort study of 656 children from the Faroe Islands. Am J Clin Nutr 99(1):5-13; doi:10.3945/ajcn.113.066720.
65. Thayer KA, Heindel JJ, Bucher JR, Gallo MA. 2012. Role of environmental chemicals in diabetes and obesity: a National Toxicology Program workshop review. Environ Health Perspect 120:779-789. doi:10.1289/ehp.1104597.
66. Tian LL, Zhao YC, Wang XC, Gu JL, Sun ZJ, Zhang YX, et al. 2009. Effects of gestational cadmium exposure on pregnancy outcome and development in the offspring at age 4.5 years. Biol Trace Elem Res 132(1-3):51-59.
67. Valvi D, Casas M, Mendez MA, Ballesteros-Gómez A, Luque N, Rubio S, et al. 2013. Prenatal bisphenol A urine concentrations and early rapid growth and overweight risk in the offspring. Epidemiology 24(6):791-799; doi:10.1097/EDE.0b013e3182a67822.
68. Valvi D, Casas M, Romaguera D, Monfort N, Ventura R, Martinez D, et al. 2015. Prenatal phthalate exposure and childhood growth and blood pressure: evidence from the Spanish INMA-Sabadell birth cohort study. Environ Health Perspect 123:1022-1029; doi:10.1289/ ehp.1408887.
69. Valvi D, Mendez MA, Garcia-Esteban R, Ballester F, Ibarluzea J, Goñi F, et al. 2014. Prenatal exposure to persistent organic pollutants and rapid weight gain and overweight in infancy. Obesity (Silver Spring) 22(2):488-496.
70. Valvi D, Mendez MA, Martinez D, Grimalt JO, Torrent M, Sunyer J, et al. 2012. Prenatal concentrations of polychlorinated biphenyls, DDE, and DDT and overweight in children: a prospective birth cohort study. Environ Health Perspect 120:451-457; doi:10.1289/ehp.1103862.
71. Verhulst SL, Nelen V, Hond ED, Koppen G, Beunckens C, Vael C, et al. 2009. Intrauterine exposure to environmental pollutants and body mass index during the first 3 years of life. Environ Health Perspect 117:122-126; doi:10.1289/ehp.0800003.
72. Wang G, Chen Z, Bartell T, Wang X. 2014. Early life origins of metabolic syndrome: the role of environmental toxicants. Curr Environ Health Rep 1(1):78-89.
73. Warner M, Aguilar Schall R, Harley KG, Bradman A, Barr D, Eskenazi B. 2013. In uteroDDT and DDE exposure and obesity status of 7-year-old MexicanAmerican children in the CHAMACOS cohort. Environ Health Perspect 121:631-636; doi:10.1289/ehp.1205656.
74. White IR, Royston P, Wood AM. 2011. Multiple imputation using chained equations: issues and guidance for practice. Stat Med 30(4):377-399.
75. WHO/UNEP (World Health Organization/United Nations Environment Programme). 2013. State-of-theScience of Endocrine Disrupting Chemicals-2012 (Bergman Å, Heindel JJ, Jobling S, Kidd KA, Zoeller RT, eds). Geneva:WHO Press. Available: http://www. who.int/ceh/publications/endocrine/en/ [accessed 13 February 2014].