Abstract
Objectives
Antenatal exposure to organic pollutants is a leading public health problem. Meconium is a unique matrix to perform prenatal studies because it enables us to retrospectively evaluate fetal exposure accumulated during the second and third trimester. The aim of the present study was to evaluate associations between organic pollutant levels in meconium and birth weight in NW Spain.
Methods
In this study, we quantify the concentrations of 50 organic pollutants together with the total values of the most important chemical groups in meconium using gas chromatography coupled to tandem mass spectrometry.
Results
Organochlorine pesticides, polychlorinated biphenyls and polybrominated diphenyl ethers were detected with the highest levels in meconium from small for gestational age newborns. It was estimated that several congeners were statistically significant (p<0.05). However, organophosphorus pesticides attained higher concentrations in newborns with an appropriate weight.
Conclusions
The occurrence of transplacental transfer can be confirmed. Prenatal exposure to organic pollutants was associated with a decrease in birth weight and, therefore, organic pollutants could have an impact on fetal growth. Nevertheless, these results need validation in larger sample sized studies.
-
Research funding: None declared.
-
Author contributions: Esther Álvarez-Silvares: Methodology, Supervision, Investigation, Formal analysis, Writing – review and editing. Tania Fernández-Cruz: Data curation, Methodology, Formal analysis. Paula Domínguez-Vigo and Paula Rubio Cid: Investigation, writing, review and editing. Elena Martínez-Carballo: Data curation, Supervision. Teresa Seoane Pillado: Formal analysis. All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
-
Competing interests: Authors state no conflict of interest.
-
Informed consent: Informed consent was obtained from all individuals included in this study.
-
Ethical approval: The study was approved by Pontevedra-Vigo-Ourense Research Ethics Committee with registry code 2014/410. The Declaration of Helsinki on biomedical research was applied at all times.
-
Data availability: The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.
References
1. Lee, PA, Chernausek, SD, Hokken-Koelega, AC, Czernichow, P. International Small for Gestational Age Advisory Board consensus development conference statement: management of short children born small for gestational age, April 24–October 1, 2001. Pediatrics 2003;111:1253–61.10.1542/peds.111.6.1253Search in Google Scholar
2. Mikolajczyk, RT, Zhang, J, Betran, AP, Souza, JP, Mori, R, Gülmezoglu, AM, et al.. A global reference for fetal-weight and birthweight percentiles. Lancet 2011;377:1855–61.10.1016/S0140-6736(11)60364-4Search in Google Scholar
3. Hwang, IT. Long-term care, from neonatal period to adulthood, of children born small for gestational age. Clin Pediatr Endocrinol 2019;28:97–103.10.1297/cpe.28.97Search in Google Scholar
4. Tatsuta, N, Kurokawa, N, Nakai, K, Suzuki, K, Iwai-Shimada, M, Murata, K, et al.. Effects of intrauterine exposures to polychlorinated biphenyls, methylmercury, and lead on birth weight in Japanese male and female newborns. Environ Health Prev Med 2017;22:39.10.1186/s12199-017-0635-6Search in Google Scholar
5. Iszatt, N, Stigum, H, Verner, MA, White, RA, Govarts, E, Murinova, LP, et al.. Prenatal and postnatal exposure to persistent organic pollutants and infant growth: a pooled analysis of seven European birth cohorts. Environ Health Perspect 2015;123:730–6.10.1289/ehp.1308005Search in Google Scholar
6. Govarts, E, Nieuwenhuijsen, M, Schoeters, G, Ballester, F, Bloemen, K, de Boer, M, et al.. Birth weight and prenatal exposure to polychlorinated biphenyls (PCBs) and dichlorodiphenyldichloroethylene (DDE): a meta-analysis within 12 European Birth Cohorts. Environ Health Perspect 2012;120:162–70.10.1289/ehp.1103767Search in Google Scholar
7. Lignell, S, Aune, M, Darnerud, PO, Hanberg, A, Larsson, SC, Glynn, A. Prenatal exposure to polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) may influence birth weight among infants in a Swedish cohort with background exposure: a cross-sectional study. Environ Health 2013;12:44.10.1186/1476-069X-12-44Search in Google Scholar
8. Fernández-Cruz, T, Martínez-Carballo, E, Simal-Gándara, J. Perspective on pre- and post-natal agro-food exposure to persistent organic pollutants and their effects on quality of life. Environ Int 2017;100:79–101.10.1016/j.envint.2017.01.001Search in Google Scholar
9. Diamanti-Kandarakis, E, Bourguignon, JP, Giudice, LC, Hauser, R, Prins, GS, Soto, AM, et al.. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 2009;30:293–342.10.1210/er.2009-0002Search in Google Scholar
10. Ostrea, EM, Morales, V, Ngoumgna, E, Prescilla, R, Tan, E, Hernandez, E, et al.. Prevalence of fetal exposure to environmental toxins as determined by meconium analysis. Neurotoxicology 2002;23:329–39.10.1016/S0161-813X(02)00077-3Search in Google Scholar
11. Fernández-Cruz, T, Álvarez-Silvares, E, Domínguez-Vigo, P, Simal-Gándara, J, Martínez-Carballo, E. Prenatal exposure to organic pollutants in northwestern Spain using noninvasive matrices (placenta and meconium). Sci Total Environ 2020;731:138341. https://doi.org/10.1016/j.scitotenv.2020.138341.Search in Google Scholar
12. Geaghan, SM. Fetal laboratory medicine: on the Frontier of maternal-fetal medicine. Clin Chem 2012;58:337–52.10.1373/clinchem.2011.166991Search in Google Scholar
13. Clark, DA. Times of first void and first stool in 500 newborns. Pediatrics 1977;60:457–9.10.1542/peds.60.4.457Search in Google Scholar
14. Harries, JT. Meconium in health and disease. Br Med Bull 1978;34:75–8.10.1093/oxfordjournals.bmb.a071462Search in Google Scholar
15. Terasaka, D, Clark, DA, Singh, BN, Rokahr, J. Free fatty acids of human meconium. Biol Neonate 1986;50:16–20.10.1159/000242556Search in Google Scholar
16. Kääpä, P, Kytölä, J, Soukka, H, Ahotupa, M. Human meconium has potent antioxidative properties. Biol Neonate 1997;72:71–5.10.1159/000244468Search in Google Scholar
17. Ortega García, JA, Carrizo Gallardo, D, Ferris i Tortajada, J, García, MM, Grimalt, JO. Meconium and neurotoxicants: searching for a prenatal exposure timing. Arch Dis Child 2006;91:642–6.10.1136/adc.2005.084129Search in Google Scholar
18. Ostrea, EMJr, Knapp, DK, Tannenbaum, L, Ostrea, AR, Romero, A, Salari, V, et al.. Estimates of illicit drug use during pregnancy by maternal interview, hair analysis, and meconium analysis. J Pediatr 2001;138:344–8.10.1067/mpd.2001.111429Search in Google Scholar
19. Ostrea, EMJr, Romero, A, Knapp, DK, Ostrea, AR, Lucena, JE, Utarnachitt, RB. Postmortem drug analysis of meconium in early-gestation human fetuses exposed to cocaine: clinical implications. J Pediatr 1994;124:477–9.10.1016/S0022-3476(94)70379-5Search in Google Scholar
20. Ryan, RM, Wagner, CL, Schultz, JM, Varley, J, DiPreta, J, Sherer, DM, et al.. Meconium analysis for improved identification of infants exposed to cocaine in utero. J Pediatr 1994;125:435–40.10.1016/S0022-3476(05)83291-3Search in Google Scholar
21. Jeong, Y, Lee, S, Kim, S, Choi, SD, Park, J, Kim, HJ, et al.. Occurrence and prenatal exposure to persistent organic pollutants using meconium in Korea: feasibility of meconium as a non-invasive human matrix. Environ Res 2016;147:8–15.10.1016/j.envres.2016.01.033Search in Google Scholar PubMed
22. Cassoulet, R, Haroune, L, Abdelouahab, N, Gillet, V, Baccarelli, AA, Cabana, H, et al.. Monitoring of prenatal exposure to organic and inorganic contaminants using meconium from an Eastern Canada cohort. Environ Res 2019;171:44–51.10.1016/j.envres.2018.12.044Search in Google Scholar PubMed PubMed Central
23. Jeong, Y, Lee, S, Kim, S, Park, J, Kim, HJ, Choi, G, et al.. Placental transfer of persistent organic pollutants and feasibility using the placenta as a non-invasive biomonitoring matrix. Sci Total Environ 2018;612:1498–505.10.1016/j.scitotenv.2017.07.054Search in Google Scholar PubMed
24. Neta, G, Goldman, LR, Barr, D, Apelberg, BJ, Witter, FR, Halden, RU. Fetal exposure to chlordane and permethrin mixtures in relation to inflammatory cytokines and birth outcomes. Environ Sci Technol 2011;45:1680–7.10.1021/es103417jSearch in Google Scholar PubMed PubMed Central
25. Tan, J, Loganath, A, Chong, YS, Obbard, JP. Exposure to persistent organic pollutants in utero and related maternal characteristics on birth outcomes: a multivariate data analysis approach. Chemosphere 2009;74:428–33.10.1016/j.chemosphere.2008.09.045Search in Google Scholar PubMed
26. Clarkson, TW. Environmental contaminants in the food chain. Am J Clin Nutr 1995;61(3 Suppl):682S–6S.10.1093/ajcn/61.3.682SSearch in Google Scholar PubMed
27. Fremlin, KM, Elliott, JE, Green, DJ, Drouillard, KG, Harner, T, Eng, A, et al.. Trophic magnification of legacy persistent organic pollutants in an urban terrestrial food web. Sci Total Environ 2020;714:136746.10.1016/j.scitotenv.2020.136746Search in Google Scholar PubMed
28. UNEP. Stockholm convention on persistent organic pollutants. Available from: http://chm.pops.int [Accessed 4 Apr 2020].Search in Google Scholar
29. Guo, H, Jin, Y, Cheng, Y, Leaderer, B, Lin, S, Holford, TR, et al.. Prenatal exposure to organochlorine pesticides and infant birth weight in China. Chemosphere 2014;110:1–7.10.1016/j.chemosphere.2014.02.017Search in Google Scholar PubMed PubMed Central
30. Ouidir, M, Buck Louis, GM, Kanner, J, Grantz, KL, Zhang, C, Sundaram, R, et al.. Association of maternal exposure to persistent organic pollutants in early pregnancy with fetal growth. JAMA Pediatr 2020;174:149–61.10.1001/jamapediatrics.2019.5104Search in Google Scholar PubMed PubMed Central
31. Weisskopf, MG, Anderson, HA, Hanrahan, LP, Kanarek, MS, Falk, CM, Steenport, DM, et al.. Maternal exposure to Great Lakes sport-caught fish and dichlorodiphenyl dichloroethylene, but not polychlorinated biphenyls, is associated with reduced birth weight. Environ Res 2005;97:149–62.10.1016/j.envres.2004.01.014Search in Google Scholar PubMed
32. Wojtyniak, BJ, Rabczenko, D, Jönsson, BA, Zvezday, V, Pedersen, HS, Rylander, L, et al.. Association of maternal serum concentrations of 2,2′, 4,4′5,5′-hexachlorobiphenyl (CB-153) and 1,1-dichloro-2,2-bis (p-chlorophenyl)-ethylene (p,p′-DDE) levels with birth weight, gestational age and preterm births in Inuit and European populations. Environ Health 2010;9:56. https://doi.org/10.1186/1476-069X-9-56.Search in Google Scholar PubMed PubMed Central
33. Alvarez-Pedrerol, M, Guxens, M, Ibarluzea, J, Rebagliato, M, Rodriguez, A, Espada, M, et al.. Organochlorine compounds, iodine intake, and thyroid hormone levels during pregnancy. Environ Sci Technol 2009;43:7909–15.10.1021/es9007273Search in Google Scholar PubMed
34. Blazer, S, Moreh-Waterman, Y, Miller-Lotan, R, Tamir, A, Hochberg, Z. Maternal hypothyroidism may affect fetal growth and neonatal thyroid function. Obstet Gynecol 2003;102:232–41.10.1097/00006250-200308000-00007Search in Google Scholar
35. Wang, Y, He, Y, Zhuang, L, Li, X, Chen, T, Chen, L, et al.. Effect of maternal and neonatal factors on neonatal thyroid screening results. Clin Lab 2018;64:1445–50.10.7754/Clin.Lab.2018.180310Search in Google Scholar PubMed
36. Liu, Y, Chen, H, Jing, C, Li, F. The association between maternal subclinical hypothyroidism and growth, development, and childhood intelligence: a meta-analysis. J Clin Res Pediatr Endocrinol 2018;10:153–61.10.4274/jcrpe.4931Search in Google Scholar PubMed PubMed Central
37. Kim, S, Park, J, Kim, HJ, Lee, JJ, Choi, G, Choi, S, et al.. Association between several persistent organic pollutants and thyroid hormone levels in cord blood serum and bloodspot of the newborn infants of Korea. PloS One 2015;10:e0125213. https://doi.org/10.1371/journal.pone.0125213.Search in Google Scholar PubMed PubMed Central
38. Gheidarloo, M, Kelishadi, R, Hovsepian, S, Keikha, M, Hashemipour, M. The association between prenatal exposure to organochlorine compounds and neonatal thyroid hormone levels: a systematic review. J Pediatr Endocrinol Metab 2020;33:21–33.10.1515/jpem-2019-0336Search in Google Scholar PubMed
39. Scollon, EJ, Carr, JA, Cobb, GP. The effect of flight, fasting and p,p′-DDT on thyroid hormones and corticosterone in Gambel’s white-crowned sparrow, Zonotrichia leucophrys gambelli. Comp Biochem Physiol C Toxicol Pharmacol 2004;137:179–89.10.1016/j.cca.2004.01.004Search in Google Scholar PubMed
40. Santini, F, Vitti, P, Ceccarini, G, Mammoli, C, Rosellini, V, Pelosini, C, et al.. In vitro assay of thyroid disruptors affecting TSH-stimulated adenylate cyclase activity. J Endocrinol Invest 2003;26:950–5.10.1007/BF03348190Search in Google Scholar PubMed
41. Waliszewski, SM, Aguirre, AA, Infanzon, RM, Silva, CS, Siliceo, J. Organochlorine pesticide levels in maternal adipose tissue, maternal blood serum, umbilical blood serum, and milk from inhabitants of Veracruz, Mexico. Arch Environ Contam Toxicol 2001;40:432–8.10.1007/s002440010194Search in Google Scholar PubMed
42. Boada, LD, Lara, PC, Alvarez-León, EE, Losada, A, Zumbado, ML, Limiñana-Cañal, JM, et al.. Serum levels of insulin-like growth factor-I in relation to organochlorine pesticides exposure. Growth Hormone IGF Res 2007;17:506–11.10.1016/j.ghir.2007.05.004Search in Google Scholar PubMed
43. Farhang, L, Weintraub, JM, Petreas, M, Eskenazi, B, Bhatia, R. Association of DDT and DDE with birth weight and length of gestation in the child health and development studies, 1959–1967. Am J Epidemiol 2005;162:717–25.10.1093/aje/kwi276Search in Google Scholar PubMed
44. Khanjani, N, Sim, MR. Maternal contamination with dichlorodiphenyltrichloroethane and reproductive outcomes in an Australian population. Environ Res 2006;101:373–9.10.1016/j.envres.2005.10.003Search in Google Scholar PubMed
45. Han, VK, Bassett, N, Walton, J, Challis, JR. The expression of insulin-like growth factor (IGF) and IGF-binding protein (IGFBP) genes in the human placenta and membranes: evidence for IGF-IGFBP interactions at the feto-maternal interface. J Clin Endocrinol Metab 1996;81:2680–93.10.1210/jcem.81.7.8675597Search in Google Scholar
46. Takeda, Y, Iwashita, M. Role of growth factors on fetal growth and maturation. Ann Acad Med Singapore 1993;22:134–41.Search in Google Scholar
47. Nawathe, AR, Christian, M, Kim, SH, Johnson, M, Savvidou, MD, Terzidou, V. Insulin-like growth factor axis in pregnancies affected by fetal growth disorders. Clin Epigenet 2016;8:11.10.1186/s13148-016-0178-5Search in Google Scholar PubMed PubMed Central
48. Fenster, L, Eskenazi, B, Anderson, M, Bradman, A, Harley, K, Hernandez, H, et al.. Association of in utero organochlorine pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect 2006;114:597–602.10.1097/00001648-200509000-00253Search in Google Scholar
49. Llop, S, Murcia, M, Iñiguez, C, Roca, M, González, L, Yusà, V, et al.. Distributions and determinants of urinary biomarkers of organophosphate pesticide exposure in a prospective Spanish birth cohort study. Environ Health 2017;16:46. https://doi.org/10.1186/s12940-017-0255-z.Search in Google Scholar PubMed PubMed Central
50. van den Dries, MA, Pronk, A, Guxens, M, Spaan, S, Voortman, T, Jaddoe, VW, et al.. Determinants of organophosphate pesticide exposure in pregnant women: a population-based cohort study in the Netherlands. Int J Hyg Environ Health 2018;221:489–501.10.1016/j.ijheh.2018.01.013Search in Google Scholar PubMed PubMed Central
51. Song, X, Seidler, FJ, Saleh, JL, Zhang, J, Padilla, S, Slotkin, TA. Cellular mechanisms for developmental toxicity of chlorpyrifos: targeting the adenylyl cyclase signaling cascade. Toxicol Appl Pharmacol 1997;145:158–74.10.1006/taap.1997.8171Search in Google Scholar PubMed
52. Campos, É, Freire, C. Exposure to non-persistent pesticides and thyroid function: a systematic review of epidemiological evidence. Int J Hyg Environ Health 2016;219:481–97.10.1016/j.ijheh.2016.05.006Search in Google Scholar PubMed
53. Eskenazi, B, Bradman, A, Castorina, R. Exposures of children to organophosphate pesticides and their potential adverse health effects. Environ Health Perspect 1999;107(3 Suppl):409–19.10.1289/ehp.99107s3409Search in Google Scholar PubMed PubMed Central
54. Jaacks, LM, Diao, N, Calafat, AM, Ospina, M, Mazumdar, M, Ibne Hasan, MOS, et al.. Association of prenatal pesticide exposures with adverse pregnancy outcomes and stunting in rural Bangladesh. Environ Int 2019;133:105243.10.1016/j.envint.2019.105243Search in Google Scholar PubMed PubMed Central
55. Kartini, A, Subagio, HW, Hadisaputro, S, Kartasurya, MI, Suhartono, S, Budiyono, B. Pesticide exposure and stunting among children in agricultural areas. Int J Occup Environ Med 2019;10:17–29.10.15171/ijoem.2019.1428Search in Google Scholar PubMed PubMed Central
56. Berkowitz, GS, Obel, J, Deych, E, Lapinski, R, Godbold, J, Liu, Z, et al.. Exposure to indoor pesticides during pregnancy in a multiethnic, urban cohort. Environ Health Perspect 2003;111:79–84.10.1289/ehp.5619Search in Google Scholar PubMed PubMed Central
57. Ferguson, KK, van den Dries, MA, Gaillard, R, Pronk, A, Spaan, S, Tiemeier, H, et al.. Organophosphate pesticide exposure in pregnancy in association with ultrasound and delivery measures of fetal growth. Environ Health Perspect 2019;127:87005.10.1289/EHP4858Search in Google Scholar PubMed PubMed Central
58. Costa, LG, Richter, RJ, Li, WF, Cole, T, Guizzetti, M, Furlong, CE. Paraoxonase (PON 1) as a biomarker of susceptibility for organophosphate toxicity. Biomarkers 2003;8:1–12.10.1080/13547500210148315Search in Google Scholar PubMed
59. Rauch, SA, Braun, JM, Barr, DB, Calafat, AM, Khoury, J, Montesano, AM, et al.. Associations of prenatal exposure to organophosphate pesticide metabolites with gestational age and birth weight. Environ Health Perspect 2012;120:1055–60. https://doi.org/10.1289/ehp.1104615.Search in Google Scholar PubMed PubMed Central
60. Harley, KG, Engel, SM, Vedar, MG, Eskenazi, B, Whyatt, RM, Lanphear, BP, et al.. Prenatal exposure to organophosphorous pesticides and fetal growth: pooled results from four longitudinal birth cohort studies. Environ Health Perspect 2016;124:1084–92.10.1289/ehp.1409362Search in Google Scholar PubMed PubMed Central
61. Koutroulakis, D, Sifakis, S, Tzatzarakis, MN, Alegakis, AK, Theodoropoulou, E, Kavvalakis, MP, et al.. Dialkyl phosphates in amniotic fluid as a biomarker of fetal exposure to organophosphates in Crete, Greece; association with fetal growth. Reprod Toxicol 2014;46:98–105.10.1016/j.reprotox.2014.03.010Search in Google Scholar PubMed
62. Dong, X, Wang, Q, Peng, J, Wu, M, Pan, B, Xing, B. Transfer of polycyclic aromatic hydrocarbons from mother to fetus in relation to pregnancy complications. Sci Total Environ 2018;636:61–8.10.1016/j.scitotenv.2018.04.274Search in Google Scholar PubMed
63. Zhang, X, Li, X, Jing, Y, Fang, X, Zhang, X, Lei, B, et al.. Transplacental transfer of polycyclic aromatic hydrocarbons in paired samples of maternal serum, umbilical cord serum, and placenta in Shanghai, China. Environ Pollut 2017;222:267–75.10.1016/j.envpol.2016.12.046Search in Google Scholar PubMed
64. Agency for Toxic Substances and Disease Registry. Toxicological profile for polycyclic aromatic hydrocarbons [Online]. Available from: https://www.atsdr.cdc.gov/toxprofiles/tp69.pdf [Accessed 14 Apr 2020].Search in Google Scholar
65. Aquilina, NJ, Delgado-Saborit, JM, Meddings, C, Baker, S, Harrison, RM, Jacob, P3rd, et al.. Environmental and biological monitoring of exposures to PAHs and ETS in the general population. Environ Int 2010;36:763–71.10.1016/j.envint.2010.05.015Search in Google Scholar PubMed PubMed Central
66. Choi, H, Jedrychowski, W, Spengler, J, Camann, DE, Whyatt, RM, Rauh, V, et al.. International studies of prenatal exposure to polycyclic aromatic hydrocarbons and fetal growth. Environ Health Perspect 2006;114:1744–50.10.1289/ehp.8982Search in Google Scholar
67. Choi, H, Wang, L, Lin, X, Spengler, JD, Perera, FP. Fetal window of vulnerability to airborne polycyclic aromatic hydrocarbons on proportional intrauterine growth restriction. PloS One 2012;7:e35464.10.1371/journal.pone.0035464Search in Google Scholar
68. Langlois, PH, Hoyt, AT, Desrosiers, TA, Lupo, PJ, Lawson, CC, Waters, MA, et al.. Maternal occupational exposure to polycyclic aromatic hydrocarbons and small for gestational age offspring. Occup Environ Med 2014;71:529–35.10.1136/oemed-2013-101833Search in Google Scholar
69. Jedrychowski, W, Perera, FP, Tang, D, Stigter, L, Mroz, E, Flak, E, et al.. Impact of barbecued meat consumed in pregnancy on birth outcomes accounting for personal prenatal exposure to airborne polycyclic aromatic hydrocarbons: birth cohort study in Poland. Nutrition 2012;28:372–7.10.1016/j.nut.2011.07.020Search in Google Scholar
70. Drwal, E, Rak, A, Gregoraszczuk, EL. Review: polycyclic aromatic hydrocarbons (PAHs)-action on placental function and health risks in future life of newborns. Toxicology 2019;411:133–42.10.1016/j.tox.2018.10.003Search in Google Scholar
71. Yamashita, F, Hayashi, M. Fetal PCB syndrome: clinical features, intrauterine growth retardation and possible alteration in calcium metabolism. Environ Health Perspect 1985;59:41–5.10.1289/ehp.59-1568075Search in Google Scholar
72. Vafeiadi, M, Vrijheid, M, Fthenou, E, Chalkiadaki, G, Rantakokko, P, Kiviranta, H, et al.. Persistent organic pollutants exposure during pregnancy, maternal gestational weight gain, and birth outcomes in the mother-child cohort in Crete, Greece (RHEA study). Environ Int 2014;64:116–23.10.1016/j.envint.2013.12.015Search in Google Scholar
73. Rylander, L, Strömberg, U, Hagmar, L. Lowered birth weight among infants born to women with a high intake of fish contaminated with persistent organochlorine compounds. Chemosphere 2000;40:1255–62.10.1016/S0045-6535(99)00377-XSearch in Google Scholar
74. Konishi, K, Sasaki, S, Kato, S, Ban, S, Washino, N, Kajiwara, J, et al.. Prenatal exposure to PCDDs/PCDFs and dioxin-like PCBs in relation to birth weight. Environ Res 2009;109:906–13.10.1016/j.envres.2009.07.010Search in Google Scholar PubMed
75. Bloom, MS, Buck Louis, GM, Schisterman, EF, Liu, A, Kostyniak, PJ. Maternal serum polychlorinated biphenyl concentrations across critical windows of human development. Environ Health Perspect 2007;115:1320–4.10.1289/ehp.10086Search in Google Scholar PubMed PubMed Central
76. Halldorsson, TI, Thorsdottir, I, Meltzer, HM, Nielsen, F, Olsen, SF. Linking exposure to polychlorinated biphenyls with fatty fish consumption and reduced fetal growth among Danish pregnant women: a cause for concern? Am J Epidemiol 2008;168:958–65.10.1093/aje/kwn204Search in Google Scholar
77. Karmaus, W, Zhu, X. Maternal concentration of polychlorinated biphenyls and dichlorodiphenyl dichlorethylene and birth weight in Michigan fish eaters: a cohort study. Environ Health 2004;3:1. https://doi.org/10.1186/1476-069X-3-1.Search in Google Scholar
78. Sagiv, SK, Tolbert, PE, Altshul, LM, Korrick, SA. Organochlorine exposures during pregnancy and infant size at birth. Epidemiology 2007;18:120–9.10.1097/01.ede.0000249769.15001.7cSearch in Google Scholar
79. Xu, X, Chiung, YM, Lu, F, Qiu, S, Ji, M, Huo, X. Associations of cadmium, bisphenol A and polychlorinated biphenyl co-exposure in utero with placental gene expression and neonatal outcomes. Reprod Toxicol 2015;52:62–70.10.1016/j.reprotox.2015.02.004Search in Google Scholar
80. Gladen, BC, Shkiryak-Nyzhnyk, ZA, Chyslovska, N, Zadorozhnaja, TD, Little, RE. Persistent organochlorine compounds and birth weight. Ann Epidemiol 2003;13:151–7.10.1016/S1047-2797(02)00268-5Search in Google Scholar
81. Longnecker, MP, Klebanoff, MA, Brock, JW, Guo, X. Maternal levels of polychlorinated biphenyls in relation to preterm and small-for-gestational-age birth. Epidemiology 2005;16:641–7.10.1097/01.ede.0000172137.45662.85Search in Google Scholar PubMed
82. Mendez, MA, Plana, E, Guxens, M, Foradada Morillo, CM, Albareda, RM, Garcia-Esteban, R, et al.. Seafood consumption in pregnancy and infant size at birth: results from a prospective Spanish cohort. J Epidemiol Community Health 2010;64:216–22. https://doi.org/10.1136/jech.2008.081893.Search in Google Scholar PubMed
83. Zou, H, Lin, Y, Yang, L, Ou, C, Geng, F, Wang, Y, et al.. Neonatal weight and prenatal exposure to polychlorinated biphenyls: a meta-analysis. Asian Pac J Cancer Prev 2019;20:3251–8. https://doi.org/10.31557/APJCP.2019.20.11.3251.Search in Google Scholar PubMed PubMed Central
84. Brouwer, A, Morse, DC, Lans, MC, Schuur, AG, Murk, AJ, Klasson-Wehler, E, et al.. Interactions of persistent environmental organohalogens with the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol Ind Health 1998;14:59–84.10.1177/074823379801400107Search in Google Scholar PubMed
85. Meeker, JD, Altshul, L, Hauser, R. Serum PCBs, p,p′-DDE and HCB predict thyroid hormone levels in men. Environ Res 2007;104:296–304.10.1016/j.envres.2006.11.007Search in Google Scholar PubMed PubMed Central
86. Abdelouahab, N, Langlois, MF, Lavoie, L, Corbin, F, Pasquier, JC, Takser, L. Maternal and cord-blood thyroid hormone levels and exposure to polybrominated diphenyl ethers and polychlorinated biphenyls during early pregnancy. Am J Epidemiol 2013;178:701–13.10.1093/aje/kwt141Search in Google Scholar PubMed
87. Forhead, AJ, Fowden, AL. Thyroid hormones in fetal growth and prepartum maturation. J Endocrinol 2014;221:R87–103.10.1530/JOE-14-0025Search in Google Scholar PubMed
88. Maervoet, J, Vermeir, G, Covaci, A, Van Larebeke, N, Koppen, G, Schoeters, G, et al.. Association of thyroid hormone concentrations with levels of organochlorine compounds in cord blood of neonates. Environ Health Perspect 2007;115:1780–6.10.1289/ehp.10486Search in Google Scholar PubMed PubMed Central
89. Tsuji, M, Aiko, Y, Kawamoto, T, Hachisuga, T, Kooriyama, C, Myoga, M, et al.. Polychlorinated biphenyls (PCBs) decrease the placental syncytiotrophoblast volume and increase Placental Growth Factor (PlGF) in the placenta of normal pregnancy. Placenta 2013;34:619–23.10.1016/j.placenta.2013.03.007Search in Google Scholar PubMed
90. Foster, WG, Gregorovich, S, Morrison, KM, Atkinson, SA, Kubwabo, C, Stewart, B, et al.. Human maternal and umbilical cord blood concentrations of polybrominated diphenyl ethers. Chemosphere 2011;84:1301–9.10.1016/j.chemosphere.2011.05.028Search in Google Scholar PubMed
91. Gómara, B, Herrero, L, Ramos, JJ, Mateo, JR, Fernández, MA, García, JF, et al.. Distribution of polybrominated diphenyl ethers in human umbilical cord serum, paternal serum, maternal serum, placentas, and breast milk from Madrid population, Spain. Environ Sci Technol 2007;41:6961–8.10.1021/es0714484Search in Google Scholar PubMed
92. Li, LX, Chen, L, Meng, XZ, Chen, BH, Chen, SQ, Zhao, Y, et al.. Exposure levels of environmental endocrine disruptors in mother-newborn pairs in China and their placental transfer characteristics. PloS One 2013;8:e62526. https://doi.org/10.1371/journal.pone.0062526.Search in Google Scholar PubMed PubMed Central
93. Lin, SM, Chen, FA, Huang, YF, Hsing, LL, Chen, LL, Wu, LS, et al.. Negative associations between PBDE levels and thyroid hormones in cord blood. Int J Hyg Environ Health 2011;214:115–20.10.1016/j.ijheh.2010.10.002Search in Google Scholar PubMed
94. Zhao, Y, Song, Q, Ge, W, Jin, Y, Chen, S, Zhao, Y, et al.. Associations between in utero exposure to polybrominated diphenyl ethers, pathophysiological state of fetal growth and placental DNA methylation changes. Environ Int 2019;133:105255. https://doi.org/10.1016/j.envint.2019.105255.Search in Google Scholar PubMed
95. Roze, E, Meijer, L, Bakker, A, Van Braeckel, KN, Sauer, PJ, Bos, AF. Prenatal exposure to organohalogens, including brominated flame retardants, influences motor, cognitive, and behavioral performance at school age. Environ Health Perspect 2009;117:1953–8.10.1289/ehp.0901015Search in Google Scholar PubMed PubMed Central
96. Ruel, MVM, Bos, AF, Soechitram, SD, Meijer, L, Sauer, PJJ, Berghuis, SA. Prenatal exposure to organohalogen compounds and children’s mental and motor development at 18 and 30 months of age. Neurotoxicology 2019;72:6–14.10.1016/j.neuro.2019.01.003Search in Google Scholar PubMed
97. Chen, A, Yolton, K, Rauch, SA, Webster, GM, Hornung, R, Sjödin, A, et al.. Prenatal polybrominated diphenyl ether exposures and neurodevelopment in U.S. children through 5 years of age: the HOME study. Environ Health Perspect 2014;122:856–62.10.1289/ehp.1307562Search in Google Scholar PubMed PubMed Central
98. Vafeiadi, M, Georgiou, V, Chalkiadaki, G, Rantakokko, P, Kiviranta, H, Karachaliou, M, et al.. Association of prenatal exposure to persistent organic pollutants with obesity and cardiometabolic traits in early childhood: the Rhea mother-child cohort (Crete, Greece). Environ Health Perspect 2015;123:1015–21.10.1289/ehp.1409062Search in Google Scholar PubMed PubMed Central
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/jpm-2020-0324).
© 2021 Walter de Gruyter GmbH, Berlin/Boston