CoChat
Sign Up
Cited by 10Effects and risks of endocrine disrupting chemicalsEpigenetics and DNA MethylationBirth, Development, and Health

Sex-Specific Associations between Prenatal Exposure to Bisphenols and Phthalates and Infant Epigenetic Age Acceleration

Open access
England-Mason, Gillian, Merrill, Sarah M., Liu, Jiaying, Martin, Jonathan W., MacDonald, Amy M., Kinniburgh, David W., Gladish, Nicole, MacIsaac, Julia L. +4 more·2024·Epigenomes
DOI 10.3390/epigenomes8030031PMC PMC11348373
Open this paper in CoChat — free accountOpen PDF

Abstract

We examined whether prenatal exposure to two classes of endocrine-disrupting chemicals (EDCs) was associated with infant epigenetic age acceleration (EAA), a DNA methylation biomarker of aging. Participants included 224 maternal–infant pairs from a Canadian pregnancy cohort study. Two bisphenols and 12 phthalate metabolites were measured in maternal second trimester urines. Buccal epithelial cell cheek swabs were collected from 3 month old infants and DNA methylation was profiled using the Infinium MethylationEPIC BeadChip. The Pediatric-Buccal-Epigenetic tool was used to estimate EAA. Sex-stratified robust regressions examined individual chemical associations with EAA, and Bayesian kernel machine regression (BKMR) examined chemical mixture effects. Adjusted robust models showed that in female infants, prenatal exposure to total bisphenol A (BPA) was positively associated with EAA (B = 0.72, 95% CI: 0.21, 1.24), and multiple phthalate metabolites were inversely associated with EAA (Bs from −0.36 to −0.66, 95% CIs from −1.28 to −0.02). BKMR showed that prenatal BPA was the most important chemical in the mixture and was positively associated with EAA in both sexes. No overall chemical mixture effects or male-specific associations were noted. These findings indicate that prenatal EDC exposures are associated with sex-specific deviations in biological aging, which may have lasting implications for child health and development.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/epigenomes8030031

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 92 · Cited by 10

Research works printed but not linked: 89

  1. [3]Frederiksen H. Skakkebaek N.E. Andersson A.-M. Metabolism of Phthalates in Humans Mol. Nutr. Food Res. 2007 51 899 911 10.1002/mnfr.200600243 17604388 · DOI · Paper page
  2. [4]Gramec Skledar D. Peterlin Mašič L. Bisphenol A and Its Analogs: Do Their Metabolites Have Endocrine Activity? Environ. Toxicol. Pharmacol. 2016 47 182 199 10.1016/j.etap.2016.09.014 27771500 · DOI
  3. [5]Arbuckle T.E. Davis K. Marro L. Fisher M. Legrand M. LeBlanc A. Gaudreau E. Foster W.G. Choeurng V. Fraser W.D. Phthalate and Bisphenol A Exposure among Pregnant Women in Canada—Results from the MIREC Study Environ. Int. 2014 68 55 65 10.1016/j.envint.2014.02.010 24709781 · DOI
  4. [6]Liu J. Wattar N. Field C.J. Dinu I. Dewey D. Martin J.W. Exposure and Dietary Sources of Bisphenol A (BPA) and BPA-Alternatives among Mothers in the APrON Cohort Study Environ. Int. 2018 119 319 326 10.1016/j.envint.2018.07.001 29990952 · DOI
  5. [7]Cantonwine D.E. Meeker J.D. Ferguson K.K. Mukherjee B. Hauser R. McElrath T.F. Urinary Concentrations of Bisphenol A and Phthalate Metabolites Measured during Pregnancy and Risk of Preeclampsia Environ. Health Perspect. 2016 124 1651 1655 10.1289/EHP188 27177253 PMC5047771 · DOI
  6. [8]Philips E.M. Trasande L. Kahn L.G. Gaillard R. Steegers E.A.P. Jaddoe V.W.V. Early Pregnancy Bisphenol and Phthalate Metabolite Levels, Maternal Hemodynamics and Gestational Hypertensive Disorders Hum. Reprod. 2019 34 365 373 10.1093/humrep/dey364 30576447 PMC6343467 · DOI
  7. [9]Mose T. Mortensen G.K. Hedegaard M. Knudsen L.E. Phthalate Monoesters in Perfusate from a Dual Placenta Perfusion System, the Placenta Tissue and Umbilical Cord Blood Reprod. Toxicol. 2007 23 83 91 10.1016/j.reprotox.2006.08.006 17049806 · DOI
  8. [11]Trasande L. Nelson M.E. Alshawabkeh A. Barrett E.S. Buckley J.P. Dabelea D. Dunlop A.L. Herbstman J.B. Meeker J.D. Naidu M. Prenatal Phthalate Exposure and Adverse Birth Outcomes in the USA: A Prospective Analysis of Births and Estimates of Attributable Burden and Costs Lancet Planet. Health 2024 8 e74 e85 10.1016/S2542-5196(23)00270-X 38331533 PMC11444077 · DOI
  9. [12]Smarr M.M. Grantz K.L. Sundaram R. Maisog J.M. Kannan K. Louis G.M.B. Parental Urinary Biomarkers of Preconception Exposure to Bisphenol A and Phthalates in Relation to Birth Outcomes Environ. Health 2015 14 73 10.1186/s12940-015-0060-5 26362861 PMC4567813 · DOI
  10. [13]Cowell W. Jacobson M.H. Long S.E. Wang Y. Kahn L.G. Ghassabian A. Naidu M. Torshizi G.D. Afanasyeva Y. Liu M. Maternal Urinary Bisphenols and Phthalates in Relation to Estimated Fetal Weight across Mid to Late Pregnancy Environ. Int. 2023 174 107922 10.1016/j.envint.2023.107922 37075581 PMC10165618 · DOI
  11. [14]Nelson W. Liu D.-Y. Yang Y. Zhong Z.-H. Wang Y.-X. Ding Y. In Utero Exposure to Persistent and Nonpersistent Endocrine-Disrupting Chemicals and Anogenital Distance. A Systematic Review of Epidemiological Studies Biol. Reprod. 2020 102 276 291 10.1093/biolre/ioz200 31621835 · DOI
  12. [15]Philippat C. Nakiwala D. Calafat A.M. Botton J. De Agostini M. Heude B. Slama R. The 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 10.1289/EHP1314 28937960 PMC5915182 · DOI
  13. [16]Dewey D. Martin J.W. MacDonald A.M. Kinniburgh D.W. Letourneau N. Giesbrecht G.F. Field C.J. Bell R.C. England-Mason G. Sex-Specific Associations between Maternal Phthalate Exposure and Neurodevelopmental Outcomes in Children at 2 Years of Age in the APrON Cohort NeuroToxicology 2023 98 48 60 10.1016/j.neuro.2023.07.005 37517784 · DOI
  14. [17]Liu J. Martin L.J. Dinu I. Field C.J. Dewey D. Martin J.W. Interaction of Prenatal Bisphenols, Maternal Nutrients, and Toxic Metal Exposures on Neurodevelopment of 2-Year-Olds in the APrON Cohort Environ. Int. 2021 155 106601 10.1016/j.envint.2021.106601 33962233 · DOI
  15. [18]Grandjean P. Barouki R. Bellinger D.C. Casteleyn L. Chadwick L.H. Cordier S. Etzel R.A. Gray K.A. Ha E.-H. Junien C. Life-Long Implications of Developmental Exposure to Environmental Stressors: New Perspectives Endocrinology 2015 156 3408 3415 10.1210/en.2015-1350 26241067 PMC4588822 · DOI
  16. [19]Solomon O. Yousefi P. Huen K. Gunier R.B. Escudero-Fung M. Barcellos L.F. Eskenazi B. Holland N. Prenatal Phthalate Exposure and Altered Patterns of DNA Methylation in Cord Blood Environ. Mol. Mutagen. 2017 58 398 410 10.1002/em.22095 28556291 PMC6488305 · DOI
  17. [20]Lee J. Kim J. Zinia S.S. Park J. Won S. Kim W.J. Prenatal Phthalate Exposure and Cord Blood DNA Methylation Sci. Rep. 2023 13 7046 10.1038/s41598-023-33002-8 37120575 PMC10148847 · DOI
  18. [21]Huang L.-L. Zhou B. Ai S.-H. Yang P. Chen Y.-J. Liu C. Deng Y.-L. Lu Q. Miao X.-P. Lu W.-Q. Prenatal Phthalate Exposure, Birth Outcomes and DNA Methylation of Alu and LINE-1 Repetitive Elements: A Pilot Study in China Chemosphere 2018 206 759 765 10.1016/j.chemosphere.2018.05.030 29793068 · DOI
  19. [22]McCabe C.F. Padmanabhan V. Dolinoy D.C. Domino S.E. Jones T.R. Bakulski K.M. Goodrich J.M. Maternal Environmental Exposure to Bisphenols and Epigenome-Wide DNA Methylation in Infant Cord Blood Environ. Epigenet. 2020 6 dvaa021 10.1093/eep/dvaa021 33391824 PMC7757124 · DOI
  20. [23]England-Mason G. Merrill S.M. Gladish N. Moore S.R. Giesbrecht G.F. Letourneau N. MacIsaac J.L. MacDonald A.M. Kinniburgh D.W. Ponsonby A.-L. Prenatal Exposure to Phthalates and Peripheral Blood and Buccal Epithelial DNA Methylation in Infants: An Epigenome-Wide Association Study Environ. Int. 2022 163 107183 10.1016/j.envint.2022.107183 35325772 · DOI
  21. [24]Miura R. Araki A. Minatoya M. Miyake K. Chen M.-L. Kobayashi S. Miyashita C. Yamamoto J. Matsumura T. Ishizuka M. An Epigenome-Wide Analysis of Cord Blood DNA Methylation Reveals Sex-Specific Effect of Exposure to Bisphenol A Sci. Rep. 2019 9 12369 10.1038/s41598-019-48916-5 31451752 PMC6710292 · DOI
  22. [25]Merrill S.M. Letourneau N. Giesbrecht G.F. Edwards K. MacIsaac J.L. Martin J.W. MacDonald A.M. Kinniburgh D.W. Kobor M.S. Dewey D. Sex-Specific Associations between Prenatal Exposure to Di(2-Ethylhexyl) Phthalate, Epigenetic Age Acceleration, and Susceptibility to Early Childhood Upper Respiratory Infections Epigenomes 2024 8 3 10.3390/epigenomes8010003 38390895 PMC10885049 · DOI
  23. [26]Horvath S. Raj K. DNA Methylation-Based Biomarkers and the Epigenetic Clock Theory of Ageing Nat. Rev. Genet. 2018 19 371 384 10.1038/s41576-018-0004-3 29643443 · DOI · Paper page
  24. [27]Wang J. Zhou W.-H. Epigenetic Clocks in the Pediatric Population: When and Why They Tick? Chin. Med. J. 2021 134 2901 2910 10.1097/CM9.0000000000001723 34520417 PMC8710336 · DOI
  25. [28]Khodasevich D. Holland N. Hubbard A. Harley K. Deardorff J. Eskenazi B. Cardenas A. Associations between Prenatal Phthalate Exposure and Childhood Epigenetic Age Acceleration Environ. Res. 2023 231 116067 10.1016/j.envres.2023.116067 37149020 PMC10330458 · DOI
  26. [29]Horvath S. DNA Methylation Age of Human Tissues and Cell Types Genome Biol. 2013 14 R115 10.1186/gb-2013-14-10-r115 24138928 PMC4015143 · DOI · Paper page
  27. [31]Lu A.T. Quach A. Wilson J.G. Reiner A.P. Aviv A. Raj K. Hou L. Baccarelli A.A. Li Y. Stewart J.D. DNA Methylation GrimAge Strongly Predicts Lifespan and Healthspan Aging 2019 11 303 327 10.18632/aging.101684 30669119 PMC6366976 · DOI · Paper page
  28. [32]Lu A.T. Binder A.M. Zhang J. Yan Q. Reiner A.P. Cox S.R. Corley J. Harris S.E. Kuo P.-L. Moore A.Z. DNA Methylation GrimAge Version 2 Aging 2022 14 9484 9549 10.18632/aging.204434 36516495 PMC9792204 · DOI
  29. [33]McEwen L.M. O’Donnell K.J. McGill M.G. Edgar R.D. Jones M.J. MacIsaac J.L. Lin D.T.S. Ramadori K. Morin A. Gladish N. The PedBE Clock Accurately Estimates DNA Methylation Age in Pediatric Buccal Cells Proc. Natl. Acad. Sci. USA 2020 117 23329 23335 10.1073/pnas.1820843116 31611402 PMC7519312 · DOI
  30. [34]Montrose L. Padmanabhan V. Goodrich J.M. Domino S.E. Treadwell M.C. Meeker J.D. Watkins D.J. Dolinoy D.C. Maternal Levels of Endocrine Disrupting Chemicals in the First Trimester of Pregnancy Are Associated with Infant Cord Blood DNA Methylation Epigenetics 2018 13 301 309 10.1080/15592294.2018.1448680 29513082 PMC5997152 · DOI
  31. [35]Song X. Zhou X. Yang F. Liang H. Wang Z. Li R. Miao M. Yuan W. Association between Prenatal Bisphenol a Exposure and Promoter Hypermethylation of CAPS2, TNFRSF25, and HKR1 Genes in Cord Blood Environ. Res. 2020 190 109996 10.1016/j.envres.2020.109996 32763279 · DOI
  32. [36]Reddy V. McCarthy M. Raval A.P. Xenoestrogens Impact Brain Estrogen Receptor Signaling during the Female Lifespan: A Precursor to Neurological Disease? Neurobiol. Dis. 2022 163 105596 10.1016/j.nbd.2021.105596 34942334 · DOI
  33. [37]Caporossi L. Papaleo B. Exposure to Bisphenol a and Gender Differences: From Rodents to Humans Evidences and Hypothesis about the Health Effects J. Xenobiot. 2015 5 5264 10.4081/xeno.2015.5264 30701039 PMC6324472 · DOI
  34. [38]Prada D. Belsky D. Baccarelli A.A. Is This Environment Making You Older? Molecular Biomarkers and New Approaches to Investigate the Influences of Environmental Chemicals through Aging Med. Lav. 2021 112 8 14 10.23749/mdl.v112i1.10826 33635291 PMC8023055 · DOI
  35. [39]Gomaa N. Konwar C. Gladish N. Au-Young S.H. Guo T. Sheng M. Merrill S.M. Kelly E. Chau V. Branson H.M. Association of Pediatric Buccal Epigenetic Age Acceleration With Adverse Neonatal Brain Growth and Neurodevelopmental Outcomes Among Children Born Very Preterm With a Neonatal Infection JAMA Netw. Open 2022 5 e2239796 10.1001/jamanetworkopen.2022.39796 36322087 PMC9631102 · DOI
  36. [40]Grohs M.N. Reynolds J.E. Liu J. Martin J.W. Pollock T. Lebel C. Dewey D. APrON Study Team Prenatal Maternal and Childhood Bisphenol a Exposure and Brain Structure and Behavior of Young Children Environ. Health 2019 18 85 10.1186/s12940-019-0528-9 31615514 PMC6794724 · DOI
  37. [41]Li C. Gao W. Gao Y. Yu C. Lv J. Lv R. Duan J. Sun Y. Guo X. Cao W. Age Prediction of Children and Adolescents Aged 6-17 Years: An Epigenome-Wide Analysis of DNA Methylation Aging 2018 10 1015 1026 10.18632/aging.101445 29754148 PMC5990383 · DOI
  38. [42]Chen C.-H. Jiang S.S. Chang I.-S. Wen H.-J. Sun C.-W. Wang S.-L. Association between Fetal Exposure to Phthalate Endocrine Disruptor and Genome-Wide DNA Methylation at Birth Environ. Res. 2018 162 261 270 10.1016/j.envres.2018.01.009 29367177 · DOI
  39. [43]Petroff R.L. Padmanabhan V. Dolinoy D.C. Watkins D.J. Ciarelli J. Haggerty D. Ruden D.M. Goodrich J.M. Prenatal Exposures to Common Phthalates and Prevalent Phthalate Alternatives and Infant DNA Methylation at Birth Front. Genet. 2022 13 793278 10.3389/fgene.2022.793278 35432478 PMC9010032 · DOI
  40. [45]Dammering F. Martins J. Dittrich K. Czamara D. Rex-Haffner M. Overfeld J. de Punder K. Buss C. Entringer S. Winter S.M. The Pediatric Buccal Epigenetic Clock Identifies Significant Ageing Acceleration in Children with Internalizing Disorder and Maltreatment Exposure Neurobiol. Stress 2021 15 100394 10.1016/j.ynstr.2021.100394 34621920 PMC8482287 · DOI
  41. [46]Verlinden I. Coppens G. Vanhorebeek I. Güiza F. Derese I. Wouters P.J. Joosten K.F. Verbruggen S.C. Van den Berghe G. Long-Term Impact of Paediatric Critical Illness on the Difference between Epigenetic and Chronological Age in Relation to Physical Growth Clin. Epigenet 2023 15 8 10.1186/s13148-023-01424-w 36639798 PMC9840263 · DOI
  42. [47]Minatoya M. Itoh S. Yamazaki K. Araki A. Miyashita C. Tamura N. Yamamoto J. Onoda Y. Ogasawara K. Matsumura T. Prenatal Exposure to Bisphenol A and Phthalates and Behavioral Problems in Children at Preschool Age: The Hokkaido Study on Environment and Children’s Health Environ. Health Prev. Med. 2018 23 43 10.1186/s12199-018-0732-1 30193567 PMC6129008 · DOI
  43. [48]Daniel S. Balalian A.A. Insel B.J. Liu X. Whyatt R.M. Calafat A.M. Rauh V.A. Perera F.P. Hoepner L.A. Herbstman J. Prenatal and Early Childhood Exposure to Phthalates and Childhood Behavior at Age 7 Years Environ. Int. 2020 143 105894 10.1016/j.envint.2020.105894 32679391 PMC7867029 · DOI
  44. [49]Yu Y. Jia Y. Liu Q. Zhao L. Lin H. Liu Z. Fang T. Jiang W. Cui H. Hou S. Prenatal Phthalate Exposure and Birth Size: A Systematic Review and Meta-Analysis Int. J. Environ. Health Res. 2023 34 2813 2829 10.1080/09603123.2023.2275645 37979196 · DOI
  45. [50]Jin S. Cui S. Xu J. Zhang X. Associations between Prenatal Exposure to Phthalates and Birth Weight: A Meta-Analysis Study Ecotoxicol. Environ. Saf. 2023 262 115207 10.1016/j.ecoenv.2023.115207 37393820 · DOI
  46. [51]Ranjit N. Siefert K. Padmanabhan V. Bisphenol-A and Disparities in Birth Outcomes: A Review and Directions for Future Research J. Perinatol. 2010 30 2 9 10.1038/jp.2009.90 19587689 PMC4028155 · DOI
  47. [52]Alisch R.S. Barwick B.G. Chopra P. Myrick L.K. Satten G.A. Conneely K.N. Warren S.T. Age-Associated DNA Methylation in Pediatric Populations Genome Res. 2012 22 623 632 10.1101/gr.125187.111 22300631 PMC3317145 · DOI
  48. [53]Pérez R.F. Santamarina P. Tejedor J.R. Urdinguio R.G. Álvarez-Pitti J. Redon P. Fernández A.F. Fraga M.F. Lurbe E. Longitudinal Genome-Wide DNA Methylation Analysis Uncovers Persistent Early-Life DNA Methylation Changes J. Transl. Med. 2019 17 15 10.1186/s12967-018-1751-9 30626398 PMC6327427 · DOI
  49. [54]Fang F. Zhou L. Perng W. Marsit C.J. Knight A.K. Cardenas A. Aung M.T. Hivert M.-F. Aris I.M. Goodrich J.M. Evaluation of Pediatric Epigenetic Clocks across Multiple Tissues Clin. Epigenet. 2023 15 142 10.1186/s13148-023-01552-3 37660147 PMC10475199 · DOI · Paper page
  50. [55]Dutta S. Goodrich J.M. Dolinoy D.C. Ruden D.M. Biological Aging Acceleration Due to Environmental Exposures: An Exciting New Direction in Toxicogenomics Research Genes 2024 15 16 10.3390/genes15010016 38275598 PMC10815440 · DOI
  51. [56]Duan R. Fu Q. Sun Y. Li Q. Epigenetic Clock: A Promising Biomarker and Practical Tool in Aging Ageing Res. Rev. 2022 81 101743 10.1016/j.arr.2022.101743 36206857 · DOI
  52. [57]Pergialiotis V. Kotrogianni P. Christopoulos-Timogiannakis E. Koutaki D. Daskalakis G. Papantoniou N. Bisphenol A and Adverse Pregnancy Outcomes: A Systematic Review of the Literature J. Matern. Fetal Neonatal Med. 2018 31 3320 3327 10.1080/14767058.2017.1368076 28805116 · DOI
  53. [58]Hu C.-Y. Li F.-L. Hua X.-G. Jiang W. Mao C. Zhang X.-J. The Association between Prenatal Bisphenol A Exposure and Birth Weight: A Meta-Analysis Reprod. Toxicol. 2018 79 21 31 10.1016/j.reprotox.2018.04.013 29709518 · DOI
  54. [59]Zhou Z. Lei Y. Wei W. Zhao Y. Jiang Y. Wang N. Li X. Chen X. Association between Prenatal Exposure to Bisphenol a and Birth Outcomes: A Systematic Review with Meta-Analysis Medicine 2019 98 e17672 10.1097/MD.0000000000017672 31689782 PMC6946218 · DOI
  55. [60]Philippat C. Mortamais M. Chevrier C. Petit C. Calafat A.M. Ye X. Silva M.J. Brambilla C. Pin I. Charles M.-A. Exposure to Phthalates and Phenols during Pregnancy and Offspring Size at Birth Environ. Health Perspect. 2012 120 464 470 10.1289/ehp.1103634 21900077 PMC3295340 · DOI
  56. [61]Pang L. Chen D. Wei H. Lan L. Li J. Xu Q. Li H. Lu C. Tang Q. Hu W. Effect of Prenatal Exposure to Phthalates on Birth Weight of Offspring: A Meta-Analysis Reprod. Toxicol. 2024 124 108532 10.1016/j.reprotox.2023.108532 38181866 · DOI
  57. [62]Wadhwa P.D. Buss C. Entringer S. Swanson J.M. Developmental Origins of Health and Disease: Brief History of the Approach and Current Focus on Epigenetic Mechanisms Semin. Reprod. Med. 2009 27 358 368 10.1055/s-0029-1237424 19711246 PMC2862635 · DOI
  58. [63]Cutfield W.S. Hofman P.L. Mitchell M. Morison I.M. Could Epigenetics Play a Role in the Developmental Origins of Health and Disease? Pediatr. Res. 2007 61 68 75 10.1203/pdr.0b013e318045764c 17413843 · DOI
  59. [64]Lourenço V.M. Pires A.M. Kirst M. Robust Linear Regression Methods in Association Studies Bioinformatics 2011 27 815 821 10.1093/bioinformatics/btr006 21217123 · DOI
  60. [65]Varin S. Panagiotakos D.B. A Review of Robust Regression in Biomedical Science Research Arch. Med. Sci. 2019 16 1267 1269 10.5114/aoms.2019.86184 32864022 PMC7444710 · DOI
  61. [66]Vernet C. Philippat C. Calafat A.M. Ye X. Lyon-Caen S. Siroux V. Schisterman E.F. Slama R. Within-Day, Between-Day, and Between-Week Variability of Urinary Concentrations of Phenol Biomarkers in Pregnant Women Environ. Health Perspect. 2018 126 037005 10.1289/EHP1994 29553460 PMC6071804 · DOI
  62. [67]Mahalingaiah S. Meeker J.D. Pearson K.R. Calafat A.M. Ye X. Petrozza J. Hauser R. Temporal Variability and Predictors of Urinary Bisphenol A Concentrations in Men and Women Environ. Health Perspect. 2008 116 173 178 10.1289/ehp.10605 18288314 PMC2235217 · DOI
  63. [68]Philips E.M. Jaddoe V.W.V. Asimakopoulos A.G. Kannan K. Steegers E.A.P. Santos S. Trasande L. Bisphenol and Phthalate Concentrations and Its Determinants among Pregnant Women in a Population-Based Cohort in the Netherlands, 2004–2005 Environ. Res. 2018 161 562 572 10.1016/j.envres.2017.11.051 29245124 PMC5820024 · DOI
  64. [69]Jessri M. Farmer A.P. Maximova K. Willows N.D. Bell R.C. APrON Study Team Predictors of Exclusive Breastfeeding: Observations from the Alberta Pregnancy Outcomes and Nutrition (APrON) Study BMC Pediatr. 2013 13 77 10.1186/1471-2431-13-77 23679578 PMC3660294 · DOI
  65. [70]Cirillo T. Latini G. Castaldi M.A. Dipaola L. Fasano E. Esposito F. Scognamiglio G. Francesco F.D. Cobellis L. Exposure to Di-2-Ethylhexyl Phthalate, Di-n-Butyl Phthalate and Bisphenol A through Infant Formulas J. Agric. Food Chem. 2015 63 3303 3310 10.1021/jf505563k 25730646 · DOI
  66. [71]Sol C.M. Gaylord A. Santos S. Jaddoe V.W.V. Felix J.F. Trasande L. Fetal Exposure to Phthalates and Bisphenols and DNA Methylation at Birth: The Generation R Study Clin. Epigenet. 2022 14 125 10.1186/s13148-022-01345-0 PMC9552446 36217170 · DOI
  67. [72]Stroheker T. Cabaton N. Nourdin G. Régnier J.-F. Lhuguenot J.-C. Chagnon M.-C. Evaluation of Anti-Androgenic Activity of Di-(2-Ethylhexyl)Phthalate Toxicology 2005 208 115 121 10.1016/j.tox.2004.11.013 15664438 · DOI
  68. [73]Takeuchi S. Iida M. Kobayashi S. Jin K. Matsuda T. Kojima H. Differential Effects of Phthalate Esters on Transcriptional Activities via Human Estrogen Receptors α and β, and Androgen Receptor Toxicology 2005 210 223 233 10.1016/j.tox.2005.02.002 15840436 · DOI
  69. [74]England-Mason G. Liu J. Martin J.W. Giesbrecht G.F. Letourneau N. Dewey D. APrON Study Team Postnatal BPA Is Associated with Increasing Executive Function Difficulties in Preschool Children Pediatr. Res. 2021 89 686 693 10.1038/s41390-020-0922-6 32408341 PMC7666018 · DOI
  70. [75]England-Mason G. Martin J.W. MacDonald A. Kinniburgh D. Giesbrecht G.F. Letourneau N. Dewey D. Similar Names, Different Results: Consistency of the Associations between Prenatal Exposure to Phthalates and Parent-Ratings of Behavior Problems in Preschool Children Environ. Int. 2020 142 105892 10.1016/j.envint.2020.105892 32593833 PMC7493743 · DOI
  71. [76]Soomro M.H. England-Mason G. Liu J. Reardon A.J.F. MacDonald A.M. Kinniburgh D.W. Martin J.W. Dewey D. APrON Study Team Associations between the Chemical Exposome and Pregnancy Induced Hypertension Environ. Res. 2023 237 116838 10.1016/j.envres.2023.116838 37544468 · DOI
  72. [77]Braun J.M. Kalkbrenner A.E. Calafat A.M. Yolton K. Ye X. Dietrich K.N. Lanphear B.P. Impact of Early-Life Bisphenol A Exposure on Behavior and Executive Function in Children Pediatrics 2011 128 873 882 10.1542/peds.2011-1335 22025598 PMC3208956 · DOI
  73. [78]Stacy S.L. Papandonatos G.D. Calafat A.M. Chen A. Yolton K. Lanphear B.P. Braun J.M. Early Life Bisphenol A Exposure and Neurobehavior at 8years of Age: Identifying Windows of Heightened Vulnerability Environ. Int. 2017 107 258 265 10.1016/j.envint.2017.07.021 28764921 PMC5567845 · DOI
  74. [79]Hornung R.W. Reed L.D. Estimation of Average Concentration in the Presence of Nondetectable Values Appl. Occup. Environ. Hyg. 1990 5 46 51 10.1080/1047322X.1990.10389587 · DOI · Paper page
  75. [80]Moran S. Arribas C. Esteller M. Validation of a DNA Methylation Microarray for 850,000 CpG Sites of the Human Genome Enriched in Enhancer Sequences Epigenomics 2016 8 389 399 10.2217/epi.15.114 26673039 PMC4864062 · DOI
  76. [82]Zheng S.C. Breeze C.E. Beck S. Dong D. Zhu T. Ma L. Ye W. Zhang G. Teschendorff A.E. EpiDISH Web Server: Epigenetic Dissection of Intra-Sample-Heterogeneity with Online GUI Bioinformatics 2020 36 1950 1951 10.1093/bioinformatics/btz833 PMC7703755 31710662 · DOI
  77. [83]Javed R. Chen W. Lin F. Liang H. Infant’s DNA Methylation Age at Birth and Epigenetic Aging Accelerators Biomed. Res. Int. 2016 2016 4515928 10.1155/2016/4515928 28058257 PMC5183755 · DOI
  78. [84]Bozack A.K. Rifas-Shiman S.L. Gold D.R. Laubach Z.M. Perng W. Hivert M.-F. Cardenas A. DNA Methylation Age at Birth and Childhood: Performance of Epigenetic Clocks and Characteristics Associated with Epigenetic Age Acceleration in the Project Viva Cohort Clin. Epigenet. 2023 15 62 10.1186/s13148-023-01480-2 37046280 PMC10099681 · DOI
  79. [85]Venables Ripley B.D. Modern Applied Statistics with S 4th ed. Springer New York City, NY, USA 2002
  80. [86]Heritier S. Cantoni E. Copt S. Victoria-Feser M.-P. Robust Methods in Biostatistics Wiley-Blackwell Hoboken, NJ, USA 2009 978-0-470-02726-4
  81. [87]Yang T. Gallagher C.M. McMahan C.S. A Robust Regression Methodology via M-Estimation Commun. Stat. Theory Methods 2019 48 1092 1107 10.1080/03610926.2018.1423698 33635297 PMC6167755 · DOI
  82. [88]Radke E.G. Braun J.M. Nachman R.M. Cooper G.S. Phthalate Exposure and Neurodevelopment: A Systematic Review and Meta-Analysis of Human Epidemiological Evidence Environ. Int. 2020 137 105408 10.1016/j.envint.2019.105408 32045779 PMC8453372 · DOI
  83. [89]Wu H. Kupsco A.J. Deierlein A.L. Just A.C. Calafat A.M. Oken E. Braun J.M. Mercado-Garcia A. Cantoral A. Téllez-Rojo M.M. Trends and Patterns of Phthalates and Phthalate Alternatives Exposure in Pregnant Women from Mexico City during 2007–2010 Environ. Sci. Technol. 2020 54 1740 1749 10.1021/acs.est.9b05836 31944681 PMC7094762 · DOI
  84. [90]Braun J.M. Li N. Arbuckle T.E. Dodds L. Massarelli I. Fraser W.D. Lanphear B.P. Muckle G. Association Between Gestational Urinary Bisphenol A Concentrations and Adiposity in Young Children: The MIREC Study Environ. Res. 2019 172 454 461 10.1016/j.envres.2019.02.038 30831435 PMC6511302 · DOI · Paper page
  85. [91]Greenland S. Daniel R. Pearce N. Outcome Modelling Strategies in Epidemiology: Traditional Methods and Basic Alternatives Int. J. Epidemiol. 2016 45 565 575 10.1093/ije/dyw040 27097747 PMC4864881 · DOI
  86. [93]Benjamini Y. Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing J. R. Stat. Society. Ser. B 1995 57 289 300 10.1111/j.2517-6161.1995.tb02031.x · DOI · Paper page
  87. [94]Bobb J.F. Valeri L. Claus Henn B. Christiani D.C. Wright R.O. Mazumdar M. Godleski J.J. Coull B.A. Bayesian Kernel Machine Regression for Estimating the Health Effects of Multi-Pollutant Mixtures Biostatistics 2015 16 493 508 10.1093/biostatistics/kxu058 25532525 PMC5963470 · DOI
  88. [95]Bobb J.F. Claus Henn B. Valeri L. Coull B.A. Statistical Software for Analyzing the Health Effects of Multiple Concurrent Exposures via Bayesian Kernel Machine Regression Environ. Health 2018 17 67 10.1186/s12940-018-0413-y 30126431 PMC6102907 · DOI
  89. [96]Bell C.G. Lowe R. Adams P.D. Baccarelli A.A. Beck S. Bell J.T. Christensen B.C. Gladyshev V.N. Heijmans B.T. Horvath S. DNA Methylation Aging Clocks: Challenges and Recommendations Genome Biol. 2019 20 249 10.1186/s13059-019-1824-y 31767039 PMC6876109 · DOI · Paper page

Authors
England-Mason, G., Merrill, S. M., Liu, J., Martin, J. W., MacDonald, A. M., Kinniburgh, D. W., Gladish, N., MacIsaac, J. L., Giesbrecht, G. F., Letourneau, N., Kobor, M. S., & Dewey, D.
Affiliations
  • University of Calgary (CA)
  • University of British Columbia (CA)
  • University of Alberta (CA)
  • Stockholm University (SE)
  • Canadian Institute for Advanced Research (CA)
Corresponding author
Dewey, Deborah
ORCID
Venue
Epigenomes
Publisher
MDPI AG
Published
2024-08-10
Volume
8
Issue
3
Pages
31
ISSN
2075-4655 (ISSN-L)
DOI
10.3390/epigenomes8030031
PMC
PMC11348373
OpenAlex
W4401509795
Cited by
10
References
92
Citations by year
2026: 4 · 2025: 5 · 2024: 1
FWCI
1.77
Type
journal article
Language
en
Open access
Licence
Locations
  • Epigenomes (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • cIRcle (University of British Columbia) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Open Collections
Funders
  • United States National Institutes of Health (1R21ES021295-01R21, PG-425614, MOP-123535, HTA-472411)
  • Canadian Institutes of Health Research (1R21ES021295-01R21, PG-425614, MOP-123535, HTA-472411)
  • CIHR Fellowship (1R21ES021295-01R21, PG-425614, MOP-123535, HTA-472411)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Keywords
prenatal exposure, bisphenol A, phthalate metabolites, endocrine disruptors, epigenetic age acceleration, DNA methylation, biological aging, sex differences, chemical mixtures, infant development

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review