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Current Obstetrics and Gynecology Reports

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01-09-2019 | Intrauterine Growth Restriction | Environmental Exposures and Pregnancy Outcomes (N Grindler, Section Editor)

Paternal Environmental Toxicant Exposure and Risk of Adverse Pregnancy Outcomes

Authors: Kaylon L. Bruner-Tran, Shilpa Mokshagundam, Alison Barlow, Tianbing Ding, Kevin G. Osteen

Published in: Current Obstetrics and Gynecology Reports | Issue 3/2019

Abstract

Purpose of Review

Current clinical efforts to predict and prevent preterm birth are primarily focused on the mother and have made minimal progress in improving outcomes. However, recent data indicate that paternal factors can also influence timing of birth. Herein, we will review recent human and murine data examining the contribution of the father to pregnancy outcomes with an emphasis on environmental exposures that can negatively impact fertility and the timing of birth.

Recent Findings

Human epidemiology studies now clearly indicate that a variety of paternal factors (age, race, weight, smoking status) can influence sperm quality, birth timing and, in some studies, offspring health. Utilizing a mouse model, our data have demonstrated that developmental exposure of the male to the environmental toxicant TCDD (2,3,7,8-tetrachlorodibenzo-p-dioxin) is associated with a transgenerational reduction in sperm number and quality and an increased risk of preterm birth in an unexposed partner.

Summary

Toxicant exposure history can clearly influence sperm quality in men and mice. Murine data further indicate that exposures which negatively affect sperm quality also impair placental function, potentially leading to preterm birth and other adverse outcomes. Of particular concern, these changes have been linked to epigenetic alterations within the male germ cell which can then be transmitted across multiple generations. Since it is not possible to prevent an ancestral toxicant exposure in a human population, identifying lifestyle modifications that can be implemented during the preconception period to improve sperm quality should be explored for the therapeutic potential to reduce the incidence of PTB and its sequelae.

Behrman RE, Butler AS, editors. Preterm Birth: Causes, Consequences, and Prevention. Washington (DC): The National Academies Collection: Reports funded by National Institutes of Health; 2007.

MarchOfDimes. Premature birth report CARD. In: 2018; 2018. https://www.marchofdimes.org/mission/prematurity-reportcard-tv.aspx. 23 May 19

• Levine H, Jorgensen N, Martino-Andrade A, Mendiola J, Weksler-Derri D, Mindlis I, et al. Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum Reprod Update. 2017;23(6):646–59. https://doi.org/10.1093/humupd/dmx022 This is a comprehensive meta-analysis identified declining sperm counts among men from North America, Europe and Australia during 1973–2011. Significantly, they identified a 50–60% decline among men unselected by fertility. CrossRefPubMedPubMedCentral

Bruner-Tran KL, Gnecco J, Ding T, Glore DR, Pensabene V, Osteen KG. Exposure to the environmental endocrine disruptor TCDD and human reproductive dysfunction: translating lessons from murine models. Reprod Toxicol. 2017;68:59–71. https://doi.org/10.1016/j.reprotox.2016.07.007.CrossRefPubMed

Ding T, McConaha M, Boyd KL, Osteen KG, Bruner-Tran KL. Developmental dioxin exposure of either parent is associated with an increased risk of preterm birth in adult mice. Reprod Toxicol. 2011;31(3):351–8. https://doi.org/10.1016/j.reprotox.2010.11.003.CrossRefPubMed

Melnick R, Lucier G, Wolfe M, Hall R, Stancel G, Prins G, et al. Summary of the National Toxicology Program's report of the endocrine disruptors low-dose peer review. Environ Health Perspect. 2002;110(4):427–31. https://doi.org/10.1289/ehp.02110427.CrossRefPubMedPubMedCentral

Tiffon C. The impact of nutrition and environmental epigenetics on human health and disease. Int J Mol Sci. 2018;19(11). https://doi.org/10.3390/ijms19113425.

Ding T, Lambert LA, Aronoff DM, Osteen KG, Bruner-Tran KL. Sex-dependent influence of developmental toxicant exposure on group B streptococcus-mediated preterm birth in a murine model. Reprod Sci. 2018;25(5):662–73. https://doi.org/10.1177/1933719117741378.CrossRefPubMed

Ding T, Mokshagundam S, Rinaudo PF, Osteen KG, Bruner-Tran KL. Paternal developmental toxicant exposure is associated with epigenetic modulation of sperm and placental Pgr and Igf2 in a mouse model. Biol Reprod. 2018;99(4):864–76. https://doi.org/10.1093/biolre/ioy111.CrossRefPubMedPubMedCentral

10.

Bruner-Tran KL, Resuehr D, Ding T, Lucas JA, Osteen KG. The role of endocrine disruptors in the epigenetics of reproductive disease and dysfunction: potential relevance to humans. Curr Obstet Gynecol Rep. 2012;1(3):116–23. https://doi.org/10.1007/s13669-012-0014-7.CrossRefPubMedPubMedCentral

11.

Skinner MK. Endocrine disruptors in 2015: epigenetic transgenerational inheritance. Nat Rev Endocrinol. 2016;12(2):68–70. https://doi.org/10.1038/nrendo.2015.206.CrossRefPubMed

12.

Lambrot R, Xu C, Saint-Phar S, Chountalos G, Cohen T, Paquet M, et al. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun. 2013;4:2889. https://doi.org/10.1038/ncomms3889.CrossRefPubMed

13.

Siklenka K, Erkek S, Godmann M, Lambrot R, McGraw S, Lafleur C, et al. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science. 2015;350(6261):aab2006. https://doi.org/10.1126/science.aab2006.CrossRefPubMed

14.

Estill MS, Krawetz SA. The epigenetic consequences of paternal exposure to environmental contaminants and reproductive toxicants. Curr Environ Health Rep. 2016;3(3):202–13. https://doi.org/10.1007/s40572-016-0101-4.CrossRefPubMed

15.

Ibrahim Y, Hotaling J. Sperm epigenetics and its impact on male fertility, pregnancy loss, and somatic health of future Offsprings. Semin Reprod Med. 2018;36(3–04):233–9. https://doi.org/10.1055/s-0038-1677047.CrossRefPubMed

16.

Barton SC, Adams CA, Norris ML, Surani MA. Development of gynogenetic and parthenogenetic inner cell mass and trophectoderm tissues in reconstituted blastocysts in the mouse. J Embryol Exp Morphol. 1985;90:267–85.PubMed

17.

Maltepe E, Fisher SJ. Placenta: the forgotten organ. Annu Rev Cell Dev Biol. 2015;31:523–52. https://doi.org/10.1146/annurev-cellbio-100814-125620.CrossRefPubMed

18.

Wang X, Miller DC, Harman R, Antczak DF, Clark AG. Paternally expressed genes predominate in the placenta. Proc Natl Acad Sci U S A. 2013;110(26):10705–10. https://doi.org/10.1073/pnas.1308998110.CrossRefPubMedPubMedCentral

19.

Houben ML, Nikkels PG, van Bleek GM, Visser GH, Rovers MM, Kessel H, et al. The association between intrauterine inflammation and spontaneous vaginal delivery at term: a cross-sectional study. PLoS One. 2009;4(8):e6572. https://doi.org/10.1371/journal.pone.0006572.CrossRefPubMedPubMedCentral

20.

Menon R, Richardson LS, Lappas M. Fetal membrane architecture, aging and inflammation in pregnancy and parturition. Placenta. 2019;79:40–5. https://doi.org/10.1016/j.placenta.2018.11.003.CrossRefPubMed

21.

Harris WS. Recent trials challenge the benefits of Omega-3. Keio J Med. 2015;64(4):65. https://doi.org/10.2302/kjm.64-003-ABST.CrossRefPubMed

22.

Jordan RG. The challenge of preterm birth. J Midwifery Womens Health. 2008;53(1):96.CrossRefPubMed

23.

McGregor JA, Allen KG, Harris MA, Reece M, Wheeler M, French JI, et al. The omega-3 story: nutritional prevention of preterm birth and other adverse pregnancy outcomes. Obstet Gynecol Surv. 2001;56(5 Suppl 1):S1–13.CrossRefPubMed

24.

• Meng Y, Groth SW. Fathers Count: The Impact of Paternal Risk Factors on Birth Outcomes. Matern Child Health J. 2018;22(3):401–8. https://doi.org/10.1007/s10995-017-2407-8 This is a retrospective cross-sectional analysis of birth certificate records (2004 to 2015) from the Finger Lakes Region in New York. Potential paternal risk factors examined included age, race/ethnicity, and education on four birth outcomes (preterm birth, low birthweight, high birthweight and small for gestational age). After controlling for maternal factors, several paternal factors (age, race, education) were found to contribute significantly to birth outcomes. CrossRefPubMedPubMedCentral

25.

Oldereid NB, Wennerholm UB, Pinborg A, Loft A, Laivuori H, Petzold M, et al. The effect of paternal factors on perinatal and paediatric outcomes: a systematic review and meta-analysis. Hum Reprod Update. 2018;24(3):320–89. https://doi.org/10.1093/humupd/dmy005.CrossRefPubMed

26.

Goisis A, Remes H, Barclay K, Martikainen P, Myrskyla M. Paternal age and the risk of low birth weight and preterm delivery: a Finnish register-based study. J Epidemiol Community Health. 2018;72(12):1104–9. https://doi.org/10.1136/jech-2017-210170.CrossRefPubMed

27.

Khandwala YS, Baker VL, Shaw GM, Stevenson DK, Lu Y, Eisenberg ML. Association of paternal age with perinatal outcomes between 2007 and 2016 in the United States: population based cohort study. BMJ. 2018;363:k4372. https://doi.org/10.1136/bmj.k4372.CrossRefPubMedPubMedCentral

28.

Palomar L, DeFranco EA, Lee KA, Allsworth JE, Muglia LJ. Paternal race is a risk factor for preterm birth. Am J Obstet Gynecol. 2007;197(2):152 e1–7. https://doi.org/10.1016/j.ajog.2007.03.035.CrossRef

29.

Shachar BZ, Mayo JA, Lyell DJ, Stevenson DK, Shaw GM, Blumenfeld YJ. Risk for spontaneous preterm birth among inter-racial/ethnic couples. J Matern Fetal Neonatal Med. 2018;31(5):633–9. https://doi.org/10.1080/14767058.2017.1293029.CrossRefPubMed

30.

Simhan HN, Krohn MA. Paternal race and preterm birth. Am J Obstet Gynecol. 2008;198(6):644 e1–6. https://doi.org/10.1016/j.ajog.2007.11.046.CrossRef

31.

Li Y, Luo Z, Holzman C, Liu H, Margerison CE. Paternal race/ethnicity and risk of adverse birth outcomes in the United States, 1989-2013. AIMS Public Health. 2018;5(3):312–23. https://doi.org/10.3934/publichealth.2018.3.312.CrossRefPubMedPubMedCentral

32.

Portha B, Grandjean V, Movassat J. Mother or father: who is in the front line? Mechanisms underlying the non-genomic transmission of obesity/diabetes via the maternal or the paternal line. Nutrients. 2019;11(2). https://doi.org/10.3390/nu11020233.

33.

Dodd JM, Du Plessis LE, Deussen AR, Grivell RM, Yelland LN, Louise J, et al. Paternal obesity modifies the effect of an antenatal lifestyle intervention in women who are overweight or obese on newborn anthropometry. Sci Rep. 2017;7(1):1557. https://doi.org/10.1038/s41598-017-01672-w.CrossRefPubMedPubMedCentral

34.

• Houfflyn S, Matthys C, Soubry A. Male Obesity: Epigenetic Origin and Effects in Sperm and Offspring. Curr Mol Biol Rep. 2017;3(4):288–96. https://doi.org/10.1007/s40610-017-0083-5 A number of recent studies have suggested or presented data indicating epigenetic changes in sperm can influence offspring health. This paper summarizes the current data on paternal obesity, molecular/epigenetic mechanisms impacting sperm and transmission of disease conditions to offspring. Perhaps of greater interest, they introduce the concept of “paternal origins of health and disease (POHaD)”. CrossRefPubMedPubMedCentral

35.

Moss JL, Harris KM. Impact of maternal and paternal preconception health on birth outcomes using prospective couples' data in add health. Arch Gynecol Obstet. 2015;291(2):287–98. https://doi.org/10.1007/s00404-014-3521-0.CrossRefPubMed

36.

Galaviz-Hernandez C, Sosa-Macias M, Teran E, Garcia-Ortiz JE, Lazalde-Ramos BP. Paternal Determinants in Preeclampsia. Front Physiol. 2018;9:1870. https://doi.org/10.3389/fphys.2018.01870.CrossRefPubMed

37.

Guo L, Choufani S, Ferreira J, Smith A, Chitayat D, Shuman C, et al. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev Biol. 2008;320(1):79–91. https://doi.org/10.1016/j.ydbio.2008.04.025.CrossRefPubMed

38.

Koukoura O, Sifakis S, Soufla G, Zaravinos A, Apostolidou S, Jones A, et al. Loss of imprinting and aberrant methylation of IGF2 in placentas from pregnancies complicated with fetal growth restriction. Int J Mol Med. 2011;28(4):481–7. https://doi.org/10.3892/ijmm.2011.754.CrossRefPubMed

39.

Koukoura O, Sifakis S, Zaravinos A, Apostolidou S, Jones A, Hajiioannou J, et al. Hypomethylation along with increased H19 expression in placentas from pregnancies complicated with fetal growth restriction. Placenta. 2011;32(1):51–7. https://doi.org/10.1016/j.placenta.2010.10.017.CrossRefPubMed

40.

He Y, Xie X, Tang W, Ma X. Maternal and paternal obesity and adverse pregnancy outcomes in China: a cohort study. Lancet. 2017. https://doi.org/10.1016/S0140-6736(17)33190-2.

41.

Goran MI, Plows JF, Ventura EE. Effects of consuming sugars and alternative sweeteners during pregnancy on maternal and child health: evidence for a secondhand sugar effect. Proc Nutr Soc. 2018;1–10. https://doi.org/10.1017/S002966511800263X.

42.

Quansah R, Jaakkola JJ. Paternal and maternal exposure to welding fumes and metal dusts or fumes and adverse pregnancy outcomes. Int Arch Occup Environ Health. 2009;82(4):529–37. https://doi.org/10.1007/s00420-008-0349-6.CrossRefPubMed

43.

Michalek JE, Rahe AJ, Boyle CA. Paternal dioxin, preterm birth, intrauterine growth retardation, and infant death. Epidemiology. 1998;9(2):161–7.CrossRefPubMed

44.

Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev. 2012;33(3):378–455. https://doi.org/10.1210/er.2011-1050.CrossRefPubMedPubMedCentral

45.

McCowan LM, North RA, Kho EM, Black MA, Chan EH, Dekker GA, et al. Paternal contribution to small for gestational age babies: a multicenter prospective study. Obesity (Silver Spring). 2011;19(5):1035–9. https://doi.org/10.1038/oby.2010.279.CrossRef

46.

Zhao L, Chen L, Yang T, Wang L, Wang T, Zhang S, et al. Parental smoking and the risk of congenital heart defects in offspring: an updated meta-analysis of observational studies. Eur J Prev Cardiol. 2019. https://doi.org/10.1177/2047487319831367.

47.

Banderali G, Martelli A, Landi M, Moretti F, Betti F, Radaelli G, et al. Short and long term health effects of parental tobacco smoking during pregnancy and lactation: a descriptive review. J Transl Med. 2015;13:327. https://doi.org/10.1186/s12967-015-0690-y.CrossRefPubMedPubMedCentral

48.

Hillman S, Peebles DM, Williams DJ. Paternal metabolic and cardiovascular risk factors for fetal growth restriction: a case-control study. Diabetes Care. 2013;36(6):1675–80. https://doi.org/10.2337/dc12-1280.CrossRefPubMedPubMedCentral

49.

Liu W, Huang C, Cai J, Wang X, Zou Z, Sun C. Household environmental exposures during gestation and birth outcomes: a cross-sectional study in Shanghai, China. Sci Total Environ. 2018;615:1110–8. https://doi.org/10.1016/j.scitotenv.2017.10.015.CrossRefPubMed

50.

Andriani H, Kuo HW. Adverse effects of parental smoking during pregnancy in urban and rural areas. BMC Pregnancy Childbirth. 2014;14:414. https://doi.org/10.1186/s12884-014-0414-y.CrossRefPubMedPubMedCentral

51.

Cui H, Gong TT, Liu CX, Wu QJ. Associations between passive maternal smoking during pregnancy and preterm birth: evidence from a meta-analysis of observational studies. PLoS One. 2016;11(1):e0147848. https://doi.org/10.1371/journal.pone.0147848.CrossRefPubMedPubMedCentral

52.

Wang L, Yang Y, Liu F, Yang A, Xu Q, Wang Q, et al. Paternal smoking and spontaneous abortion: a population-based retrospective cohort study among non-smoking women aged 20-49 years in rural China. J Epidemiol Community Health. 2018;72(9):783–9. https://doi.org/10.1136/jech-2017-210311.CrossRefPubMed

53.

Beszterda M, Franski R. Endocrine disruptor compounds in environment: as a danger for children health. Pediatr Endocrinol Diabetes Metab. 2018;24(2):88–95. https://doi.org/10.18544/PEDM-24.02.0107.CrossRefPubMed

54.

Gonzalez N, Marques M, Nadal M, Domingo JL. Occurrence of environmental pollutants in foodstuffs: a review of organic vs. conventional food. Food Chem Toxicol. 2019;125:370–5. https://doi.org/10.1016/j.fct.2019.01.021.CrossRefPubMed

55.

Zennegg M. Dioxins and PCBs in meat - still a matter of concern? Chimia (Aarau). 2018;72(10):690–6. https://doi.org/10.2533/chimia.2018.690.CrossRef

56.

Stillerman KP, Mattison DR, Giudice LC, Woodruff TJ. Environmental exposures and adverse pregnancy outcomes: a review of the science. Reprod Sci. 2008;15(7):631–50. https://doi.org/10.1177/1933719108322436.CrossRefPubMed

57.

Candela S, Bonvicini L, Ranzi A, Baldacchini F, Broccoli S, Cordioli M, et al. Exposure to emissions from municipal solid waste incinerators and miscarriages: a multisite study of the MONITER project. Environ Int. 2015;78:51–60. https://doi.org/10.1016/j.envint.2014.12.008.CrossRefPubMed

58.

Hansen DA, Esakky P, Drury A, Lamb L, Moley KH. The aryl hydrocarbon receptor is important for proper seminiferous tubule architecture and sperm development in mice. Biol Reprod. 2014;90(1):8. https://doi.org/10.1095/biolreprod.113.108845.CrossRefPubMed

59.

Hernandez-Ochoa I, Karman BN, Flaws JA. The role of the aryl hydrocarbon receptor in the female reproductive system. Biochem Pharmacol. 2009;77(4):547–59. https://doi.org/10.1016/j.bcp.2008.09.037.CrossRefPubMed

60.

Lawrence BP, Vorderstrasse BA. New insights into the aryl hydrocarbon receptor as a modulator of host responses to infection. Semin Immunopathol. 2013;35(6):615–26. https://doi.org/10.1007/s00281-013-0395-3.CrossRefPubMed

61.

Mukerjee D. Health impact of polychlorinated dibenzo-p-dioxins: a critical review. J Air Waste Manag Assoc. 1998;48(2):157–65.CrossRefPubMed

62.

Emond C, Michalek JE, Birnbaum LS, DeVito MJ. Comparison of the use of a physiologically based pharmacokinetic model and a classical pharmacokinetic model for dioxin exposure assessments. Environ Health Perspect. 2005;113(12):1666–8. https://doi.org/10.1289/ehp.8016.CrossRefPubMedPubMedCentral

63.

White SS, Birnbaum LS. An overview of the effects of dioxins and dioxin-like compounds on vertebrates, as documented in human and ecological epidemiology. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2009;27(4):197–211. https://doi.org/10.1080/10590500903310047.CrossRefPubMedPubMedCentral

64.

Pesatori AC, Consonni D, Bachetti S, Zocchetti C, Bonzini M, Baccarelli A, et al. Short- and long-term morbidity and mortality in the population exposed to dioxin after the "Seveso accident". Ind Health. 2003;41(3):127–38.CrossRefPubMed

65.

Eskenazi B, Warner M, Brambilla P, Signorini S, Ames J, Mocarelli P. The Seveso accident: a look at 40years of health research and beyond. Environ Int. 2018;121(Pt 1:71–84. https://doi.org/10.1016/j.envint.2018.08.051.CrossRefPubMedPubMedCentral

66.

Mocarelli P, Gerthoux PM, Needham LL, Patterson DG Jr, Limonta G, Falbo R, et al. Perinatal exposure to low doses of dioxin can permanently impair human semen quality. Environ Health Perspect. 2011;119(5):713–8. https://doi.org/10.1289/ehp.1002134.CrossRefPubMedPubMedCentral

67.

Mocarelli P, Gerthoux PM, Patterson DG Jr, Milani S, Limonta G, Bertona M, et al. Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality. Environ Health Perspect. 2008;116(1):70–7. https://doi.org/10.1289/ehp.10399.CrossRefPubMed

68.

Aurell J, Gullett BK, Yamamoto D. Emissions from open burning of simulated military waste from forward operating bases. Environ Sci Technol. 2012;46(20):11004–12. https://doi.org/10.1021/es303131k.CrossRefPubMed

69.

Doucet I. Desert storm syndrome: sick soldiers and dead children? Med War. 1994;10(3):183–94.CrossRefPubMed

70.

Emmerova M, Jirava F. Is gulf War syndrome really a mystery? Med Confl Surviv. 2004;20(3):209–17. https://doi.org/10.1080/1362369042000248811.CrossRefPubMed

71.

Woodall BD, Yamamoto DP, Gullett BK, Touati A. Emissions from small-scale burns of simulated deployed U.S. military waste. Environ Sci Technol. 2012;46(20):10997–1003. https://doi.org/10.1021/es3021556.CrossRefPubMed

72.

Butler DA, Styka AN, Savitz DA, editors. Assessment of the Department of Veterans Affairs Airborne Hazards and Open Burn Pit Registry. Washington (DC); 2017.

73.

Lewis J. Smokey Bear in Vietnam. Environ Hist. 2006;11(3):598–603.CrossRef

74.

Institute Of Medicine. Veterans and agent Orange: health effects of herbicides used in Vietnam. Washington, DC: National Academies Press; 1994.

75.

Ornstein C, Fresques H. ProPublica, Hixenbaugh M. The children of agent Orange. Virginia-pilot. 2016. https://www.propublica.org/article/the-children-of-agent-orange. 23 May 19

76.

Peterson B. Vietnam War veterans' kids say agent Orange impact 'a nightmare'. 2018. https://abcnews.go.com/Politics/vietnam-war-veterans-kids-agent-orange-impact-nightmare/story?id=59059570. 23 May 19

77.

WFLA. Agent Orange effects being seen in grandchildren of Vietnam War veterans. 2018. https://www.wfla.com/8-on-your-side/investigations/impacts-being-seen-in-grandchildren-of-vietnam-war-veterans-is-it-agent-orange-/1183887612. 23 May 19

78.

Part 2: Making women and men. In Johnson M, editor. Essential reproduction. Wiley; 2010.

79.

Skinner MK. What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol. 2008;25(1):2–6. https://doi.org/10.1016/j.reprotox.2007.09.001.CrossRefPubMed

80.

U.S. War Dog Association. Vietnam Statistics. http://www.uswardogs.org/vietnam-statistics/. 15 April 19

81.

Stellman JM, Stellman SD. Agent Orange during the Vietnam War: the lingering issue of its civilian and military health impact. Am J Public Health. 2018;108(6):726–8. https://doi.org/10.2105/AJPH.2018.304426.CrossRefPubMedPubMedCentral

82.

Anh NT, Nishijo M, Tai PT, Maruzeni S, Morikawa Y, Anh TH, et al. Maternal risk factors associated with increased dioxin concentrations in breast milk in a hot spot of dioxin contamination in Vietnam. J Expo Sci Environ Epidemiol. 2014;24(5):489–96. https://doi.org/10.1038/jes.2013.73.CrossRefPubMed

83.

Nghi TN, Nishijo M, Manh HD, Tai PT, Van Luong H, Anh TH, et al. Dioxins and Nonortho PCBs in breast Milk of Vietnamese mothers living in the largest hot spot of dioxin contamination. Environ Sci Technol. 2015;49(9):5732–42. https://doi.org/10.1021/es506211p.CrossRefPubMed

84.

Schecter A, Pavuk M, Constable JD, Daile C, Papke O. A follow-up: high level of dioxin contamination in Vietnamese from agent orange, three decades after the end of spraying. J Occup Environ Med. 2002;44(3):218–20.CrossRefPubMed

85.

Tai PT, Nishijo M, Anh NT, Maruzeni S, Nakagawa H, Van Luong H, et al. Dioxin exposure in breast milk and infant neurodevelopment in Vietnam. Occup Environ Med. 2013;70(9):656–62. https://doi.org/10.1136/oemed-2012-101021.CrossRefPubMed

86.

Ngo TH, Hien TT, Thuan NT, Minh NH, Chi KH. Atmospheric PCDD/F concentration and source apportionment in typical rural, agent Orange hotspots, and industrial areas in Vietnam. Chemosphere. 2017;182:647–55. https://doi.org/10.1016/j.chemosphere.2017.05.050.CrossRefPubMed

87.

Bruner-Tran KL, Osteen KG. Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod Toxicol. 2011;31(3):344–50. https://doi.org/10.1016/j.reprotox.2010.10.003.CrossRefPubMed

88.

Bruner-Tran KL, Ding T, Yeoman KB, Archibong A, Arosh JA, Osteen KG. Developmental exposure of mice to dioxin promotes transgenerational testicular inflammation and an increased risk of preterm birth in unexposed mating partners. PLoS One. 2014;9(8):e105084. https://doi.org/10.1371/journal.pone.0105084.CrossRefPubMedPubMedCentral

89.

McConaha ME, Ding T, Lucas JA, Arosh JA, Osteen KG, Bruner-Tran KL. Preconception omega-3 fatty acid supplementation of adult male mice with a history of developmental 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure prevents preterm birth in unexposed female partners. Reproduction. 2011;142(2):235–41. https://doi.org/10.1530/REP-11-0070.CrossRefPubMedPubMedCentral

90.

Zeng Y, Chen T. DNA methylation reprogramming during mammalian development. Genes (Basel). 2019;10(4). https://doi.org/10.3390/genes10040257.

91.

Koutsaki M, Sifakis S, Zaravinos A, Koutroulakis D, Koukoura O, Spandidos DA. Decreased placental expression of hPGH, IGF-I and IGFBP-1 in pregnancies complicated by fetal growth restriction. Growth Hormon IGF Res. 2011;21(1):31–6. https://doi.org/10.1016/j.ghir.2010.12.002.CrossRef

92.

Kadakia R, Josefson J. The relationship of insulin-like growth factor 2 to fetal growth and adiposity. Horm Res Paediatr. 2016;85(2):75–82. https://doi.org/10.1159/000443500.CrossRefPubMed

93.

Rogero MM, Calder PC. Obesity, inflammation, toll-like receptor 4 and fatty acids. Nutrients. 2018;10(4). https://doi.org/10.3390/nu10040432.

94.

Calder PC. Omega-3 polyunsaturated fatty acids and inflammatory processes: nutrition or pharmacology? Br J Clin Pharmacol. 2013;75(3):645–62. https://doi.org/10.1111/j.1365-2125.2012.04374.x.CrossRefPubMedPubMedCentral

95.

Massiera F, Barbry P, Guesnet P, Joly A, Luquet S, Moreilhon-Brest C, et al. A Western-like fat diet is sufficient to induce a gradual enhancement in fat mass over generations. J Lipid Res. 2010;51(8):2352–61. https://doi.org/10.1194/jlr.M006866.CrossRefPubMedPubMedCentral

96.

Hadley EE, Richardson LS, Torloni MR, Menon R. Gestational tissue inflammatory biomarkers at term labor: a systematic review of literature. Am J Reprod Immunol. 2018;79(2):e12776. https://doi.org/10.1111/aji.12776.CrossRef

97.

Burris HH, Baccarelli AA, Wright RO, Wright RJ. Epigenetics: linking social and environmental exposures to preterm birth. Pediatr Res. 2016;79(1–2):136–40. https://doi.org/10.1038/pr.2015.191.CrossRefPubMed

98.

Nieuwenhuijsen MJ, Dadvand P, Grellier J, Martinez D, Vrijheid M. Environmental risk factors of pregnancy outcomes: a summary of recent meta-analyses of epidemiological studies. Environ Health. 2013;12:6. https://doi.org/10.1186/1476-069X-12-6.CrossRefPubMedPubMedCentral

99.

Porpora MG, Piacenti I, Scaramuzzino S, Masciullo L, Rech F, Benedetti Panici P. Environmental contaminants exposure and preterm birth: a systematic review. Toxics. 2019;7(1). https://doi.org/10.3390/toxics7010011.

100.

Kumar S, Sharma S, Thaker R. Occupational, environmental, and lifestyle factors and their contribution to preterm birth - an overview. Indian J Occup Environ Med. 2017;21(1):9–17. https://doi.org/10.4103/ijoem.IJOEM_155_16.CrossRefPubMedPubMedCentral

Title: Paternal Environmental Toxicant Exposure and Risk of Adverse Pregnancy Outcomes
Authors: Kaylon L. Bruner-Tran
Shilpa Mokshagundam
Alison Barlow
Tianbing Ding
Kevin G. Osteen
Publication date: 01-09-2019
Publisher: Springer US
Keywords: Intrauterine Growth Restriction
Premature Birth
Epigenetics
Published in: Current Obstetrics and Gynecology Reports / Issue 3/2019
Electronic ISSN: 2161-3303
DOI: https://doi.org/10.1007/s13669-019-00265-w

At a glance: The STEP trials

Springer Medicine

Paternal Environmental Toxicant Exposure and Risk of Adverse Pregnancy Outcomes

Abstract

Purpose of Review

Recent Findings

Summary

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose of Review

Recent Findings

Summary

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