The role of xenobiotic-metabolizing enzymes in the placenta: a growing research field

References

• Tetro N, Moushaev S, Rubinchik-Stern M, et al. The placental barrier: the gate and the fate in drug distribution. Pharm Res. 2018;35(4):71.
   PubMed Web of Science ®Google Scholar
• Storvik M, Huuskonen P, Pehkonen P, et al. The unique characteristics of the placental transcriptome and the hormonal metabolism enzymes in placenta. Reprod Toxicol. 2014;47:9–14.
   PubMed Web of Science ®Google Scholar
• Collier AC, Thévenon AD, Goh W, et al. Placental profiling of UGT1A enzyme expression and activity and interactions with preeclampsia at term. Eur J Drug Metab Pharmacokinet. 2015;40(4):471–480.
   PubMed Web of Science ®Google Scholar
• Audus KL. Controlling drug delivery across the placenta. Eur J Pharm Sci. 1999;8(3):161–165.
   PubMed Web of Science ®Google Scholar
• Mitchell AA, Gilboa SM, Werler MM, et al. Medication use during pregnancy, with particular focus on prescription drugs 1976–2008. Am J Obstet Gynecol. 2011;205(51):e1–e8.
   PubMedGoogle Scholar
• Etwel F, Hutson JR, Madadi P, et al. Fetal and perinatal exposure to drugs and chemicals: novel biomarkers of risk. Annu Rev Pharmacol Toxicol. 2014;54:295–315.
   PubMed Web of Science ®Google Scholar
• Buhimschi CS, Weiner CP. Medications in pregnancy and lactation: part 1. Teratol Obstet Gynecol. 2009;113:166–188.
   PubMed Web of Science ®Google Scholar
• Lacroix I, Damase-Michel C, Lapeyre-Mestre M, et al. Prescription of drugs during pregnancy in France. Lancet. 2000;356:1735–1736.
   PubMed Web of Science ®Google Scholar
• Andrade SE, Gurwitz JH, Davis RL, et al. Prescription drug use in pregnancy. Am J Obstet Gynaecol. 2004;191:398–407.
   PubMed Web of Science ®Google Scholar
• De Jong LT. Van den berg PB. A study of drug utilization during pregnancy in the light of known risks. Int J Risk Safety Med. 1990;1:91–105.
   PubMedGoogle Scholar
• Richards N, Reith D, Stitely M, et al. Antiepileptic drug exposure in pregnancy and pregnancy outcome from national drug usage data. BMC Pregnancy Childbirth. 2018;18(1):1–8.
   PubMedGoogle Scholar
• Finkelstein N. Treatment programming for alcohol and drug-depend women. Int J Addict. 1993;28:1275–1309.
   PubMed Web of Science ®Google Scholar
• Tong V, Jones J, Dietz P, et al. Pregnancy risk assessment monitoring system (PRAMS), United States, 2000-2005. Morb Mortal Wkly Rep. 2009;58:1.
   PubMedGoogle Scholar
• Moore KL, Persaud TVN. The placenta and fetal membranes. In: The developing human: clinically oriented embryology. Philadelphia(PA): Saunders W.B. Co Inc; 2008. p. 110–144.
   Google Scholar
• Burton GJ, Fowden AL, Thornburg KL. Placental origins of chronic disease. Physiol Rev. 2016;96(4):1509–1565.
   PubMed Web of Science ®Google Scholar
• Costa MA. The endocrine function of human placenta: an overview. Reprod Biomed Online. 2016;32(1):14–43.
   PubMed Web of Science ®Google Scholar
• Griffiths S, Campbell J. Placental structure, function and drug transfer. BJA Educ. 2015;15(2):84–89.
   Web of Science ®Google Scholar
• Carter AM, Enders AC. Comparative aspects of trophoblast development and placentation. Reprod Biol Endocrinol. 2004;2:46.
   PubMedGoogle Scholar
• Syme MR, Paxton JW, Keelan JA, et al. Metabolism by the human placenta. Clin Pharmacokinet. 2004;43(8):487–514.
   PubMed Web of Science ®Google Scholar
• Joshi AA, Vaidya SS, St-Pierre MV, et al. Placental ABC transporters: biological impact and pharmaceutical significance. Pharm Res. 2016;33:2847–2878.
   PubMed Web of Science ®Google Scholar
• Prouillac C, Lecoeur S. The role of the placenta in fetal exposure to xenobiotics: importance of membrane transporters and human models for transfer studies. Drug Metab Dispos. 2010;38(10):1623–1635.
   PubMed Web of Science ®Google Scholar
• Staud F, Cerveny L, Ceckova M. Pharmacotherapy in pregnancy; effect of ABC and SLC transporters on drug transport across the placenta and fetal drug exposure. J Drug Target. 2012;20(9):736–763.
   PubMed Web of Science ®Google Scholar
• Kalliokoski A, Niemi M. Impact of OATP transporters on pharmacokinetics. Br J Pharmacol. 2009;158:693–705.
   PubMed Web of Science ®Google Scholar
• Fromm MF. P-glycoprotein: a defense mechanism limiting oral bioavailability and CNS accumulation of drugs. Int J Clin Pharmacol Ther. 2000;38:69–74.
   PubMed Web of Science ®Google Scholar
• Lye P, Bloise E, Nadeem L, et al. Glucocorticoids modulate multidrug resistance transporters in the first trimester human placenta. J Cell Mol Med. 2018;22(7):3652–3660.
   PubMed Web of Science ®Google Scholar
• Afrouzian M, Al-Lahham R, Patrikeeva S, et al. Role of the efflux transporters bcrp and mrp1 in human placental bio-disposition of pravastatin. Biochem Pharmacol. 2018;156:467–478.
   PubMed Web of Science ®Google Scholar
• Daud AN, Bergman JE, Bakker MK, et al. P-glycoprotein-mediated drug interactions in pregnancy and changes in the risk of congenital anomalies: a case-reference study. Drug Saf. 2015;38:651–659.
   PubMed Web of Science ®Google Scholar
• Welch RM, Harrison YE, Conney AH, et al. Cigarette smoking: stimulatory effect on metabolism of 3,4-benzpyrene by enzymes in human placenta. Science. 1968;160(3827):541–542. 3.
   PubMed Web of Science ®Google Scholar
• Vähäkangas K, Raunio H, Pasanen M, et al. Comparison of the formation of benzo[a]pyrene diolepoxide-DNA adducts in vitro by rat and human microsomes: evidence for the involvement of P-450IA1 and P-450IA2. J Biochem Toxicol. 1989;4(2):79–86.
   PubMedGoogle Scholar
• Pasanen M, Pelkonen O. Xenobiotic and steroid-metabolizing monooxygenases catalysed by cytochrome P450 and glutathione-S-transferase conjugations in the human placenta and their relationships to maternal cigarette smoking. Placenta. 1990;11:75–85.
   PubMed Web of Science ®Google Scholar
• Pacifici GM, Rane A. Epoxide hydrolase in human placenta at different stages of pregnancy. Dev Pharmacol Ther. 1983;6(2):83–93.
   PubMedGoogle Scholar
• Polidoro G, Di Ilio C, Del Boccio G, et al. Glutathione S-transferase activity in human placenta. Biochem Pharmacol. 1980;29(12):1677–1680.
   PubMed Web of Science ®Google Scholar
• Pacifici GM, Rane A. Glutathione S-epoxidetransferase in the human placenta at different stages of pregnancy. Drug Metab Dispos. 1981;9(5):472–475.
   PubMed Web of Science ®Google Scholar
• LO D, Koren G. Biotransformation of carcinogenic arylamines and arylamides by human placenta. J Lab Clin Med. 1994;124(1):134–141.
   PubMed Web of Science ®Google Scholar
• Smelt VA, Mardon HJ, Redman CW, et al. Acetylation of arylamines by the placenta. Eur J Drug Metab Pharmacokinet. 1997;22(4):403–408.
   PubMed Web of Science ®Google Scholar
• Smelt VA, Upton A, Adjaye J, et al. Expression of arylamine N-acetyltransferases in pre-term placentas and in human pre-implantation embryos. Hum Mol Genet. 2000;9:1101–1107.
   PubMed Web of Science ®Google Scholar
• Zhu L, Lu L, Wang S et al. Developing solid oral dosage forms. pharmaceutical theory and practice 2nd. Chapter 11, oral absorption basics: pathways and physicochemical and biological factors affecting absorption. Burlington (MA):Pharmaceutical Theory and Practice Burlington (MA): Elsevier Academic Press; 2017 p. 297–329.
   Google Scholar
• Pasanen M. The expression and regulation of drug metabolism in human placenta. Adv Drug Deliv Rev. 1999;38:81–97.
   PubMed Web of Science ®Google Scholar
• Pasanen M, Pelkonen O. The expression and environmental regulation of P450 enzymes in human placenta. Crit Rev Toxicol. 1994;24:211–229.
   PubMed Web of Science ®Google Scholar
• Cizkova K, Tauber Z. Time-dependent expression pattern of cytochrome P450 epoxygenases and soluble epoxide hydrolase in normal human placenta. Acta Histochem. 2018;120(6):513–519.
   PubMed Web of Science ®Google Scholar
• Hakkola J, Pasanen M, Hukkanen J, et al. Expression of xenobiotic-metabolizing cytochrome P450 forms in human full-term placenta. Biochem Pharmacol. 1996;51(4):403–411.
   PubMed Web of Science ®Google Scholar
• Hakkola J, Raunio H, Purkunen R, et al. Detection of cytochrome P450 gene expression in human placenta in first trimester of pregnancy. Biochem Pharmacol. 1996;52(2):379–383.
   PubMed Web of Science ®Google Scholar
• Avery ML, Meek CE, Audusa KL. The presence of inducible cytochrome P450 types 1A1 and 1A2 in the bewo cell line. Placenta. 2003;24:45–52.
   PubMed Web of Science ®Google Scholar
• Hakkola J, Pasanen M, Pelkonen O, et al. Expression of CYP1B1 in human adult and fetal tissues and differential inducibility of CYP1B1 and CYP1A1 by Ah receptor ligands in human placenta and cultured cells. Carcinogenesis. 1997;18(2):391–397.
   PubMed Web of Science ®Google Scholar
• Bieche I, Narjoz C, Asselah T, et al. Reverse transcriptase-PCR quantification of mRNA levels from cytochrome (CYP)1, CYP2 and CYP3 families in 22 different human tissues. Pharmacogenet Genomics. 2007;17(9):731–742.
   PubMed Web of Science ®Google Scholar
• McRobie DJ, Glover DD, Tracy TS. Effects of gestational and overt diabetes on human placental cytochromes P450 and glutathione S-transferase. Drug Metab Dispos. 1998;26(4):367–371.
   PubMed Web of Science ®Google Scholar
• Collier AC, Tingle MD, Paxton JW, et al. Metabolizing enzyme localization and activities in the first trimester human placenta: the effect of maternal and gestational age, smoking and alcohol consumption. Hum Reprod. 2002;10:2564–2572.
   Google Scholar
• Herse F, Lamarca B, Hubel CA, et al. Cytochrome P450 subfamily 2J polypeptide 2 expression and circulating epoxyeicosatrienoic metabolites in preeclampsia. Circulation. 2012;126(25):2990–2999.
   PubMed Web of Science ®Google Scholar
• Maezawa K, Matsunaga T, Takezawa T, et al. Cytochrome P450 3As gene expression and testosterone 6 beta-hydrolase activity in human fetal membranes and placenta at full term. Biol Pharm Bull. 2010;33:249–254.
   PubMed Web of Science ®Google Scholar
• Nishimura M, Yaguti H, Yoshitsugu H, et al. Tissue distribution of mRNA expression of human cytochrome P450 isoforms assessed by high-sensitivity real-time reverse transcription PCR. Yakugaku Zasshi. 2003;123:369–375.
   PubMed Web of Science ®Google Scholar
• Dalle Vedove F, Fava C, Jiang H, et al. Increased epoxyeicosatrienoic acids and reduced soluble epoxide hydrolase expression in the preeclamptic placenta. J Hypertens. 2016;34(7):1364–1370.
   PubMed Web of Science ®Google Scholar
• Wixtrom RN, Silva MH, Hammock BD. Cytosolic epoxide hydrolase in human placenta. Placenta. 1988;9(5):559–563.
   PubMed Web of Science ®Google Scholar
• Nishimura M, Naito S. Tissue-specific mRNA expression profiles of human phase I metabolizing enzymes except for cytochrome P450 and phase II metabolizing enzymes. Drug Metab Pharmacokinet. 2006;21(5):357–374.
   PubMed Web of Science ®Google Scholar
• Aiso S, Yasuda K, Shiozawa M, et al. Preparation of monoclonal antibodies to glutathione S-transferase-pi and application to immunohistochemical study. J Histochem Cytochem. 1989;7(8):1247–1252.
   Google Scholar
• Reimers A, Ostby L, Stuen I, et al. Expression of UDP glucuronosyl transferase 1A4 in human placenta at term. Eur J Drug Metab Pharmacokinet. 2011;35(3–4):79–82.
   PubMed Web of Science ®Google Scholar
• Collier AC, Keelan JA, Van Zijl PE, et al. Human placental glucuronidation and transport of 3’azido-3’-deoxythymidine and uridine diphosphate glucuronic acid. Drug Metab Dispos Biol Fate Chem. 2004;32:813–820.
   PubMed Web of Science ®Google Scholar
• Stanley EL, Hume R, Visser TJ, et al. Differential expression of sulfotransferase enzymes involved in thyroid hormone metabolism during human placental development. J Clin Endocrinol Metab. 2001;86:5944–5955.
   PubMed Web of Science ®Google Scholar
• He D, Meloche CA, Dumas NA, et al. Different subcellular localization of sulphotransferase 2B1b in human placenta and prostate. Biochem J. 2004;379(Pt 3):533–540.
   PubMedGoogle Scholar
• Whyatt RM, Bell DA, Jedrychowski W, et al. Polycyclic aromatic hydrocarbon-DNA adducts in human placenta and modulation by CYP1A1 induction and genotype. Carcinogenesis. 1998;19(8):1389–1392.
   PubMed Web of Science ®Google Scholar
• Mohammed AM, Karttunen V, Huuskonen P, et al. Transplacental transfer and metabolism of diuron in human placenta. Toxicol Lett. 2018;295:307–313.
   PubMed Web of Science ®Google Scholar
• Gallagher JE, Everson RB, Lewtas J, et al. Comparison of DNA adduct levels in human placenta from polychlorinated biphenyl exposed women and smokers in which CYP 1A1 levels are similarly elevated. Teratog Carcinog Mutagen. 1994;14(4):183–192.
   PubMedGoogle Scholar
• Stejskalová L, Vrzal R, Rulcová A, et al. Effects of glucocorticoids on cytochrome P450 1A1 (CYP1A1) expression in isolated human placental trophoblast. J Appl Biomed. 2013;11:163–172.
   Web of Science ®Google Scholar
• Janssen BG, Gyselaers W, Byun HM, et al. Placental mitochondrial DNA and CYP1A1 gene methylation as molecular signatures for tobacco smoke exposure in pregnant women and the relevance for birth weight. J Transl Med. 2017;15(1):5.
   PubMedGoogle Scholar
• Myllynen P, Pasanen M, Vähäkangas K. The fate and effects of xenobiotics in human placenta. Expert Opin Drug Metab Toxicol. 2007;3(3):331–346.
   PubMed Web of Science ®Google Scholar
• Czekaj P, Wiaderkiewicz A, Florek E, et al. Tobacco smoke-dependent changes in cytochrome P450 1A1, 1A2, and 2E1 protein expressions in fetuses, newborns, pregnant rats, and human placenta. Arch Toxicol. 2005;79(1):13–24.
   PubMed Web of Science ®Google Scholar
• Rasheed A, Hines RN, McCarver-May DG. Variation in induction of human placental CYP2E1: possible role is susceptibility to fetal alcohol syndrome. Toxicol Appl Pharmacol. 1997;144:396–400.
   PubMed Web of Science ®Google Scholar
• Schuetz JD, Kauma S, Guzelian PS. Identification of the fetal liver cytochrome CYP3A7 in human endometrium and placenta. J Clin Invest. 1993;92:1018–1024.
   PubMed Web of Science ®Google Scholar
• Huuskonen P, Amezaga MR, Bellingham M, et al. The human placental proteome is affected by maternal smoking. Reprod Toxicol. 2016;63:22–31.
   PubMed Web of Science ®Google Scholar
• Sawada M, Kitamura R, Norose T, et al. Metabolic activation of aflatoxin B1 by human placental microsomes. J Toxicol Sci. 1993;18:129–132.
   PubMedGoogle Scholar
• Storvik M, Huuskonen P, Kyllönen T, et al. Aflatoxin B1--a potential endocrine disruptor--up-regulates CYP19A1 in JEG-3 cells. Toxicol Lett. 2011;202(3):161–167.
   PubMed Web of Science ®Google Scholar
• Zharikova OL, Fokina VM, Nanovskaya TN, et al. Identification of the major human hepatic and placental enzymes responsible for the biotransformation of glyburide. Biochem Pharmacol. 2009;78:1483–1490.
   PubMed Web of Science ®Google Scholar
• Deshmukh SV, Nanovskaya TN, Ahmed MS. Aromatase is the major enzyme metabolizing buprenorphine in human placenta. J Pharmacol Exp Ther. 2003;306:1099–1105.
   PubMed Web of Science ®Google Scholar
• Nanovskaya TN, Deshmukh SV, Nekhayeva IA, et al. Methadone metabolism by human placenta. Biochem Pharmacol. 2004;68:583–591.
   PubMed Web of Science ®Google Scholar
• Spector AA, Fang X, Snyder GD, et al. Epoxyeicosatrienoic acids (EETs): metabolism and biochemical function. Prog Lipid Res. 2004;43(1):55–90.
   PubMed Web of Science ®Google Scholar
• Schäfer WR, Zahradnik HP, Arbogast E, et al. Arachidonate metabolism in human placenta, fetal membranes, decidua and myometrium: lipoxygenase and cytochrome P450 metabolites as main products in HPLC profiles. Placenta. 1996;17(4):231–238.
   PubMed Web of Science ®Google Scholar
• Hayes JD, Flanagan JU, Jowsey IR. Glutathione transferases. Annu Rev Pharmacol Toxicol. 2005;45:51–88.
   PubMed Web of Science ®Google Scholar
• Guthenberg C, Glutathione S-transferase MB. (transferase pi) from human placenta is identical or closely related to glutathione S-transferase (transferase rho) from erythrocytes. Biochim Biophys Acta. 1981;661(2):255–260.
   PubMedGoogle Scholar
• Allocati N, Masulli M, Di Ilio C, et al. Glutathione transferases: substrates, inhibitors and pro-drugs in cancer and neurodegenerative diseases. Oncogenesis. 2018;7:8.
   PubMed Web of Science ®Google Scholar
• Dalmizrak O, Kulaksiz-Erkmen G, Ozer N. Fluoxetine-induced toxicity results in human placental glutathione S-transferase-π (GST-π) dysfunction. Drug Chem Toxicol. 2016;39(4):439–444.
   PubMed Web of Science ®Google Scholar
• McRobie DJ, Glover DD, Tracy TS. Effects of gestational and overt diabetes on human placental cytochromes P450 and glutathione S-transferase. Drug Metab Dispos. 1998;26(4):367–371.
   PubMed Web of Science ®Google Scholar
• Gharesi-Fard B, Zolghadri J, Kamali-Sarvestani E. lteration in the expression of proteins in unexplained recurrent pregnancy loss compared with in the normal placenta. J Reprod Dev. 2014;60(4):261–267.
   PubMed Web of Science ®Google Scholar
• Mackenzie PI, Bock KW, Burchell B, et al. Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet Genomics. 2005;15:677–685.
   PubMed Web of Science ®Google Scholar
• Meech R, Mackenzie PI. UGT3A: novel UDP-glycosyltransferases of the UGT superfamily. Drug Metab Rev. 2010;42:45–54.
   PubMed Web of Science ®Google Scholar
• Collier AC, Ganley NA, Tingle MD, et al. UDP-glucuronosyltransferase activity, expression and cellular localization in human placenta at term. Biochem Pharmacol. 2002;63:409–419.
   PubMed Web of Science ®Google Scholar
• Coughtrie MWH. Function and organization of the human cytosolic sulfotransferase (SULT) family. Chem Biol Interact. 2016;25(259): 2–7. (PtA).
   Google Scholar
• Falany CN, He D, Dumas N, et al. Human cytosolic sulfotransferase 2B1: isoform expression, tissue specificity and subcellular localization. J Steroid Biochem Mol Biol. 2006;102:214–221.
   PubMed Web of Science ®Google Scholar
• Pavek P, Dvorak Z. Xenobiotic-induced transcriptional regulation of xenobiotic metabolizing enzymes of the cytochrome P450 superfamily in human extrahepatic tissues. Curr Drug Metab. 2008;9:129–143.
   PubMed Web of Science ®Google Scholar
• Pavek P, Smutny T. Nuclear receptors in regulation of biotransformation enzymes and drug transporters in the placental barrier. Drug Metab Rev. 2014;46(1):19–32.
   PubMed Web of Science ®Google Scholar
• Wakx A, Nedder M, Tomkiewicz-Raulet C, et al. Expression, localization, and activity of the aryl hydrocarbon receptor in the human placenta. Int J Mol Sci. 2018;19:3762.
   Web of Science ®Google Scholar
• Stejskalova L, Vecerova L, Peréz LM, et al. Aryl hydrocarbon receptor and aryl hydrocarbon nuclear translocator expression in human and rat placentas and transcription activity in human trophoblast cultures. Toxicol Sci. 2011;123(1):26–36.
   PubMed Web of Science ®Google Scholar
• Yamamoto J, Ihara K, Nakayama H, et al. Characteristic expression of aryl hydrocarbon receptor repressor gene in human tissues: organ-specific distribution and variable induction patterns in mononuclear cells. Life Sci. 2004;74(8):1039–1049.
   PubMed Web of Science ®Google Scholar
• Kolwankar D, Glover DD, Ware JA, et al. Expression and function of ABCB1 and ABCG2 in human placental tissue. Drug Metab Dispos. 2005;33:524–529.
   PubMed Web of Science ®Google Scholar
• Seok Heo J, Lim J, Pyo S, et al. Environmental benzopyrene attenuates stemness of placenta-derived mesenchymal stem cells via aryl hydrocarbon receptor. Stem Cells Int. 2019;2019:1–12.
   Web of Science ®Google Scholar
• Saif Z, Hodyl NA, Stark MJ, et al. Expression of eight glucocorticoid receptor isoforms in the human preterm placenta vary with fetal sex and birthweight. Placenta. 2015;36(7):723–730.
   PubMed Web of Science ®Google Scholar
• Johnson RF, Rennie N, Murphy V, et al. Expression of glucocorticoid receptor messenger ribonucleic acid transcripts in the human placenta at term. J Clin Endocrinol Metab. 2008;93(12):4887–4893.
   PubMed Web of Science ®Google Scholar
• Lee MJ, Wang Z, Yee H, et al. Expression and regulation of glucocorticoid receptor in human placental villous fibroblasts. Endocrinology. 2005;146:4619–4626.
   PubMed Web of Science ®Google Scholar
• Pavek P, Cerveny L, Svecova L, et al. Examination of glucocorticoid receptor alpha-mediated transcriptional regulation of P-glycoprotein, CYP3A4, and CYP2C9 genes in placental trophoblast cell lines. Placenta. 2007;28(10):1004–1011.
   PubMed Web of Science ®Google Scholar
• Pospechova K, Rozehnal V, Stejskalova L, et al. Expression and activity of vitamin D receptor in the human placenta and in choriocarcinoma BeWo and JEG-3 cell lines. Mol Cell Endocrinol. 2009;299:178–187.
   PubMed Web of Science ®Google Scholar
• Olesya B, Margarita B, Irina K, et al. Expression of vitamin D and vitamin D receptor in chorionic villous in missed abortion. Gynecological Endocrinol. 2009;35:49–55.
   Google Scholar
• Wilkens MR, Maté LM, Schnepel N, et al. Influence of 25-hydroxyvitamin D3 and 1,25-dihydroxyvitamin D3 on expression of P-glycoprotein and cytochrome P450 3A in sheep. J Steroid Biochem Mol Biol. 2016;164:271–276.
   PubMed Web of Science ®Google Scholar
• Geenes VL, Dixon PH, Chambers J, et al. Characterization of the nuclear receptors FXR, PXR and CAR in normal and cholestatic placenta. Placenta. 2011;32:535–537.
   PubMed Web of Science ®Google Scholar
• Mir ODegrelle SA, et al. Chemotherapy in pregnancy: exploratory study of the effects of paclitaxel on the expression of placental drug transporters. Investig New Drugs. 2018;37(5):1–11.
   PubMed Web of Science ®Google Scholar
• Murayama N, Kazuki Y, Satoh D, et al. Induction of human cytochrome P450 3A enzymes in cultured placental cells by thalidomide and relevance to bioactivation and toxicity. J Toxicol Sci. 2017;42(3):343–348.
   PubMed Web of Science ®Google Scholar
• Collier AC, Helliwell RJ, Keelan JA, et al. 3´-Azido-3´-deoxythymidine (AZT) induces apoptosis and alters metabolic enzyme activity in human placenta. Toxicol Appl Pharmacol. 2003;192:164–173.
   PubMed Web of Science ®Google Scholar
• Rubinchik-Stern M, Shmuel M, Eyal S. Antiepileptic drugs alter the expression of placental carriers: an in vitro study in a human placental cell line. Epilepsia. 2015;56(7):1023–1032.
   PubMed Web of Science ®Google Scholar
• Shmuel MBar J, et al. Adverse placental effects of valproic acid: studies in perfused human placentas. Epilepsia. 2018;59(5):1–11.
   Web of Science ®Google Scholar
• Kurosawa Y, Furugen A, Nishimura, et al. Evaluation of the effects of antiepileptic drugs on folic acid uptake by human placental choriocarcinoma cells. Toxicol In Vitro. 2018;48:104–110.
   PubMed Web of Science ®Google Scholar
• Neradugomma NK, Liao MZ, Buprenorphine MQ. Norbuprenorphine, R-methadone, and s-methadone upregulate BCRP/ABCG2 expression by activating aryl hydrocarbon receptor in human placental trophoblasts. Mol Pharmacol. 2017;91(3):237–249.
   PubMed Web of Science ®Google Scholar
• Reznicek J, Ceckova M, Tupova L, et al. Etravirine inhibits ABCG2 drug transporter and affects transplacental passage of tenofovir disoproxil fumarate. Placenta. 2016;47:124–129.
   PubMed Web of Science ®Google Scholar
• Patterson TA, Binienda ZK, Lipe GW, et al. Transplacental pharmacokinetics and fetal distribution of azidothymidine, its glucuronide, and phosphorylated metabolites in late-term rhesus macaques after maternal infusion. Drug Metab Dispos. 1997;25(4):453–459.
   PubMed Web of Science ®Google Scholar
• Liebes L, Mendoza S, Lee JD, et al. Further observations on zidovudine transfer and metabolism by human placenta. AIDS. 1993;7(4):590–592.
   PubMed Web of Science ®Google Scholar
• Hankins GD, Lowery CLJ, Scott RT, et al. Transplacental transfer of zidovudine in the near-term pregnant baboon. Am J Obstet Gynecol. 1990;163(3):728–732.
   PubMed Web of Science ®Google Scholar
• Nanovskaya T, Deshmukh S, Brooks M, et al. Transplacental transfer and metabolism of buprenorphine. J Pharmacol Exp Ther. 2002;300(1):26–33.
   PubMed Web of Science ®Google Scholar
• Concheiro M, Shakleya DM, Huestis MA. Simultaneous quantification of buprenorphine, norbuprenorphine, buprenorphine-glucuronide and norbuprenorphine-glucuronide in human umbilical cord by liquid chromatography tandem mass spectrometry. Forensic Sci Int. 2009;188(1–3):144–151.
   PubMed Web of Science ®Google Scholar
• Kacinko SL, Jones HE, Johnson RE, et al. Correlations of maternal buprenorphine dose, buprenorphine, and metabolite concentrations in meconium with neonatal outcomes. Clin Pharmacol Ther. 2008;84(5):604–612.
   PubMed Web of Science ®Google Scholar
• Concheiro M, Jones HE, Johnson RE, et al. Maternal buprenorphine dose, placenta buprenorphine, and metabolite concentrations and neonatal outcomes. Ther Drug Monit. 2010;32(2):206–215.
   PubMed Web of Science ®Google Scholar
• Wang X, Abdelrahman DR, Zharikova OL, et al. Bupropion metabolism by human placenta. Biochem Pharmacol. 2010;79(11):1684–1690.
   PubMed Web of Science ®Google Scholar
• Earhart AD, Patrikeeva S, Wang X, et al. Transplacental transfer and metabolism of bupropion. J Matern Fetal Neonatal Med. 2010;23(5):409–416.
   PubMed Web of Science ®Google Scholar
• Fokina VM, West H, Oncken C, et al. Bupropion therapy during pregnancy: the drug and its major metabolites in umbilical cord plasma and amniotic fluid. Am J Obstet Gynecol. 2016;215(4):497.e1-7.
   PubMed Web of Science ®Google Scholar
• Ravindran S, Zharikova OL, Hill RA, et al. Identification of glyburide metabolites formed by hepatic and placental microsomes of humans and baboons. Biochem Pharmacol. 2006;72(12):1730–1737.
   PubMed Web of Science ®Google Scholar
• Jain S, Zharikova OL, Ravindram S, et al. Glyburide metabolism by placentas of healthy and gestational diabetics. Ahmed Am J Perinatol. 2008;25(3):169–174.
   PubMed Web of Science ®Google Scholar
• de Castro A, Jones HE, Johnson RE, et al. Methadone, cocaine, opiates, and metabolite disposition in umbilical cord and correlations to maternal methadone dose and neonatal outcomes. Ther Drug Monit. 2011a;33(4):443–452.
   PubMed Web of Science ®Google Scholar
• Deshmukh SV, Nanovskaya TN, Hankins GD, et al. N-demethylation of levo-alpha-acetylmethadol by human placental aromatase. Biochem Pharmacol. 2004;67(5):885–892.
   PubMed Web of Science ®Google Scholar
• Balakrishnan B, Thorstensen EB, Ponnampalam AP, et al. Transplacental transfer and biotransformation of genistein in human placenta. Placenta. 2010;31(6):506–511.
   PubMed Web of Science ®Google Scholar
• Schenker S, Yang Y, Mattiuz E, et al. Olanzapine transfer by human placenta. Clin Exp Pharmacol Physiol. 1999;26(9):691–697.
   PubMed Web of Science ®Google Scholar
• Myllynen P, Pienimäki P, Raunio H, et al. Microsomal metabolism of carbamazepine and oxcarbazepine in liver and placenta. Hum Exp Toxicol. 1998;17(12):668–676.
   PubMed Web of Science ®Google Scholar
• Pienimäki P, Lampela E, Hakkola J, et al. Pharmacokinetics of oxcarbazepine and carbamazepine in human placenta. Epilepsia. 1997;38:309–316.
   PubMed Web of Science ®Google Scholar
• Myllynen P, Pienimäki P, Jouppila P, et al. Transplacental passage of oxcarbazepine and its metabolites in vivo. Epilepsia. 2001;42(11):1482–1485.
   PubMed Web of Science ®Google Scholar
• Pohorecki R, Rayburn W, Coon WW, et al. Some factors affecting phencyclidine biotransformation by human liver and placenta. Drug Metab Dispos. 1989;17(3):271–274.
   PubMed Web of Science ®Google Scholar
• Rayburn WF, Holsztynska EF, Domino EF. Phencyclidine: biotransformation by the human placenta. Am J Obstet Gynecol. 1984;148(1):111–112.
   PubMed Web of Science ®Google Scholar
• Sodha RJ, Schneider H. Transplacental transfer of beta-adrenergic drugs studied by an in vitro perfusion method of an isolated human placental lobule. Am J Obstet Gynecol. 1983;147(3):303–310.
   PubMed Web of Science ®Google Scholar
• Sodha RJ, Proegler M, Schneider H. Transfer and metabolism of norepinephrine studied from maternal-to-fetal and fetal-to-maternal sides in the in vitro perfused human placental lobe. Am J Obstet Gynecol. 1984;148(4):474–481.
   PubMed Web of Science ®Google Scholar
• Borrisud M, O´Shaughnessy R, Alexander MS, et al. Metabolism and disposition of ritodrine in a pregnant baboon. Am J Obstet Gynecol. 1985;152(8):1067–1072.
   PubMed Web of Science ®Google Scholar
• Rettie AE, Heimark L, Mayer RT, et al. Stereoselective and regioselective hydroxylation of warfarin and selective O-dealkylation of phenoxazone ethers in human placenta. Biochem Biophys Res Commun. 1985;126(3):1013–1021.
   PubMed Web of Science ®Google Scholar
• Juchau MR, Zachariah PK. Comparative studies on the oxidation and reduction of drug substrates in human placental versus rat hepatic microsomes. Biochem Pharmacol. 1975;24:227–233.
   PubMed Web of Science ®Google Scholar
• Karttunen V, Myllynen P, Prochazka G, et al. Placental transfer and DNA binding of benzo(a)pyrene in human placental perfusion. Toxicol Lett. 2010;197(2):75–81.
   PubMed Web of Science ®Google Scholar
• Manchester DK, Bowman ED, Parker NB, et al. Determinants of polycyclic aromatic hydrocarbon-DNA adducts in human placenta. Cancer Res. 1992;52(6):1499–1503.
   PubMed Web of Science ®Google Scholar
• Tang D, Li TY, Liu JJ, et al. PAH-DNA adducts in cord blood and fetal and child development in a Chinese cohort. Environ Health Perspect. 2006;114(8):1297–1300.
   PubMed Web of Science ®Google Scholar
• Topinka J, Milcova A, Libalova H, et al. Biomarkers of exposure to tobacco smoke and environmental pollutants in mothers and their transplacental transfer to the foetus. Mutat Res. 2009;669(1–2):13–19.
   PubMed Web of Science ®Google Scholar
• Juchau MR, Namkung MJ, Jones AH, et al. Biotransformation and bioactivation of 7,12-dimethylbenz[a]anthracene in human fetal and placental tissues. Analyses of HPLC profiles and studies with salmonella typhimurium. Drug Metab Dispos. 1978;6(3):273–281.
   PubMed Web of Science ®Google Scholar
• Lamplugh SM, Hendrickse RG, Apeagyei F, et al. Aflatoxins in breast milk, neonatal cord blood, and serum of pregnant women. Br Med J (Clin Res Ed). 1988;296(6627):968.
   PubMedGoogle Scholar
• Denning DW, Allen R, Wilkinson AP, et al. Transplacental transfer of aflatoxin in humans. Carcinogenesis. 1990;11(6):1033–1035.
   PubMed Web of Science ®Google Scholar
• Datta K, Kulkarni AP. Oxidative metabolism of aflatoxin B1 by lipoxygenase purified from human term placenta and intrauterine conceptual tissues. Teratology. 1994;50(4):311–317.
   PubMedGoogle Scholar
• Partanen HA, El-Nezami HS, Leppänen JM, et al. Aflatoxin B1 transfer and metabolism in human placenta. Toxicol Sci. 2010;113(1):216–225.
   PubMed Web of Science ®Google Scholar
• Murthy KR, Joseph P, Kulkarni AP. 2‐aminofluorene bioactivation by human term placental peroxidase. Teratog Carcinog Mutagen. 1995;15:3.
   Google Scholar
• Derewlany LO, Knie B, Koren G. Human placental transfer and metabolism of p-aminobenzoic acid. J Pharmacol Exp Ther. 1994;269(2):761–765.
   PubMed Web of Science ®Google Scholar
• Gerona RR, Woodruff TJDickenson CA, et al. Bisphenol-a (bpa), bpa glucuronide, and bpa sulfate in midgestation umbilical cord serum in a northern and central california population. Environ Sci Technol. 2013;47(21):12477–12485.
   PubMed Web of Science ®Google Scholar
• Liu J, Li J, Wu Y, et al. Bisphenol A metabolites and bisphenol s in paired maternal and cord serum. Environ Sci Technol. 2017;51(4):2456–2463.
   PubMed Web of Science ®Google Scholar
• Concheiro M, González-Colmenero E, Lendoiro E, et al. Alternative matrices for cocaine, heroin, and methadone in utero drug exposure detection. Ther Drug Monit. 2013;35(4):502–509.
   PubMed Web of Science ®Google Scholar
• Concheiro M, Lendoiro E, de Castro A, et al. Bioanalysis for cocaine, opiates, methadone, and amphetamines exposure detection during pregnancy. Drug Test Anal. 2017;9(6):898–904.
   PubMed Web of Science ®Google Scholar
• Joya X, Marchei E, Salat-Batlle J, et al. Drugs of abuse in maternal hair and paired neonatal meconium: an objective assessment of foetal exposure to gestational consumption. Drug Test Anal. 2016;8(8):864–868.
   PubMed Web of Science ®Google Scholar
• Parés X, Farrés J, Vallee BL. Organ specific alcohol metabolism: placental chi-ADH. Biochem Biophys Res Commun. 1984;119(3):1047–1055.
   PubMed Web of Science ®Google Scholar
• Andersson S, Halmesmäki E, Koivusalo M, et al. Placental alcohol metabolism in chronic alcohol abuse. Biol Neonate. 1989;56(2):90–93.
   PubMedGoogle Scholar
• Karl PI, Gordon BH, Lieber CS, et al. Acetaldehyde production and transfer by the perfused human placental cotyledon. Science. 1988;242(4876):273–275.
   PubMed Web of Science ®Google Scholar
• Brien JF, Loomis CW, Tranmer J, et al. Disposition of ethanol in human maternal venous blood and amniotic fluid. Am J Obstet Gynecol. 1983;146(2):181–186.
   PubMed Web of Science ®Google Scholar
• Collazo NR, Sultatos LG. Metabolism of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK) in human placental microsomes. Biochem Pharmacol. 1995;50(11):1933–1941.
   PubMed Web of Science ®Google Scholar
• Atalla A, Maser E. Characterization of enzymes participating in carbonyl reduction of 4-methylnitrosamino-1-(3-pyridyl)-1-butanone (NNK) in human placenta. Chem Biol Interact. 2001;130–132(1–3):737–748.
   PubMed Web of Science ®Google Scholar
• Chowdhury G, Murayama N, Okada Y, et al. Human liver microsomal cytochrome P450 3A enzymes involved in thalidomide 5-hydroxylation and formation of a glutathione conjugate. Chem Res Toxicol. 2010;23(6):1018–1024.
   PubMed Web of Science ®Google Scholar
• Kazuki Y, Akita M, Kobayashi K, et al. Thalidomide-induced limb abnormalities in a humanized CYP3A mouse model. Sci Rep. 2016;6:21419.
   PubMed Web of Science ®Google Scholar
• Zharikova OL, Ravindran S, Nanovskaya TN, et al. Kinetics of glyburide metabolism by hepatic and placental microsomes of human and baboon. Biochem Pharmacol. 2007;73(12):2012–2019.
   PubMed Web of Science ®Google Scholar
• Malek R, Davis SN. Pharmacokinetics, efficacy and safety of glyburide for treatment of gestational diabetes mellitus. Expert Opin Drug Metab Toxicol. 2016;12:691–699.
   PubMed Web of Science ®Google Scholar
• Hernández S, Catalán-García M, Morén C, et al. Placental mitochondrial toxicity, oxidative stress, apoptosis, and adverse perinatal outcomes in hiv pregnancies under antiretroviral treatment containing zidovudine. J Acquir Immune Defic Syndr. 2017;75:113–119.
   Web of Science ®Google Scholar
• Strydom K, Gerhardus-Nel D, Dhansay MA, et al. The effect of maternal HIV status and treatment duration on body composition of HIV-exposed and HIV-unexposed preterm, very and extremely low-birthweight infants. Paediatr Int Child Health. 2018;38(3):163–174.
   PubMed Web of Science ®Google Scholar
• Çetinkaya M, Özkan H, Köksal N. Unilateral radius aplasia due to lamotrigine and oxcarbazepine use in pregnancy. Matern Fetal Neonatal Med. 2008;21(12):927–930.
   PubMed Web of Science ®Google Scholar
• Schütz H, Feldmann KF, Faigle JW, et al. The metabolism of 14C oxcarbazepine in man. Xenobiotica. 1986;16(8):769–778.
   PubMed Web of Science ®Google Scholar
• Montouris G. Safety of the newer antiepileptic drug oxcarbazepine during pregnancy. Curr Med Res Opin. 2005;21:693–701.
   PubMed Web of Science ®Google Scholar
• Burnell JC, Li TK, Bosron WF. Purification and steady-state kinetic characterization of human liver beta 3 beta 3 alcohol dehydrogenase. Biochemistry. 1989;28(17):6810–6815.
   PubMed Web of Science ®Google Scholar
• Teschke R, Gellert J. Hepatic microsomal ethanol-oxidizing system (MEOS): metabolic aspects and clinical implications. Alcohol Clin Exp Res. 1986;10(6):20S–32S.
   PubMed Web of Science ®Google Scholar
• Agarwal DP. Genetic polymorphisms of alcohol metabolizing enzymes. Pathol Biol. 2001;49(9):703–709.
   PubMedGoogle Scholar
• Lieber CS, DeCarli LM. The role of the hepatic microsomal ethanol oxidizing system (MEOS) for ethanol metabolism in vivo. J Pharmacol Exp Ther. 1972;181(2):279–287.
   PubMedGoogle Scholar
• Salihu HM, Kornosky JL, Lynch O, et al. Impact of prenatal alcohol consumption on placenta-associated syndromes. Alcohol. 2011;45(1):73–79.
   PubMed Web of Science ®Google Scholar
• Lui S, Jones RL, Robinson NJ, et al. Detrimental effects of ethanol and its metabolite acetaldehyde, on first trimester human placental cell turnover and function. PLOS One. 2014;9(2):87328.
   Web of Science ®Google Scholar
• Burd L, Blair J, Dropps K. Prenatal alcohol exposure, blood alcohol concentrations and alcohol elimination rates for the mother, fetus and newborn. J Perinatol. 2012;32:652–659.
   PubMed Web of Science ®Google Scholar
• Kvigne VL, Leonardson GR, Neff-Smith M, et al. Characteristics of children who have full or incomplete fetal alcohol syndrome. J Pediatr. 2004;145(5):635–640.
   PubMed Web of Science ®Google Scholar
• Taylor CL, Jones KL, Jones MC, et al. Incidence of renal anomalies in children prenatally exposed to ethanol. Pediatrics. 1994;94(2 Pt 1):209–212.
   PubMed Web of Science ®Google Scholar
• Tai M, Piskorski A, Kao JC, et al. Placental morphology in fetal alcohol spectrum disorders. Alcohol Alcohol. 2017;52(2):138–144.
   PubMed Web of Science ®Google Scholar
• Marbury MC, Linn S, Monson R, et al. The association of alcohol consumption with outcome of pregnancy. Am J Public Health. 1983;73(10):1165–1168.
   PubMed Web of Science ®Google Scholar
• Kalisch-Smith JI, Moritz KM. Detrimental effects of alcohol exposure around conception: putative mechanisms. Biochem Cell Biol. 2018;96(2):107–116.
   PubMedGoogle Scholar
• Roe DA, Little BB, Bawdon RE, et al. Metabolism of cocaine by human placentas: implications for fetal exposure. Am J Obstet Gynecol. 1990;163(3):715–718.
   PubMed Web of Science ®Google Scholar
• Simone C, Derewlany LO, Oskamp M, et al. Acetylcholinesterase and butyrylcholinesterase activity in the human term placenta: implications for fetal cocaine exposure. J Lab Clin Med. 1994a;123(3):400–406.
   PubMed Web of Science ®Google Scholar
• Schenker S, Yang Y, Johnson RF, et al. The transfer of cocaine and its metabolites across the term human placenta. Clin Pharmacol Ther. 1993;53(3):329–339.
   PubMed Web of Science ®Google Scholar
• Simone C, Derewlany LO, Oskamp M, et al. Transfer of cocaine and benzoylecgonine across the perfused human placental cotyledon. Am J Obstet Gynecol. 1994b;170(5 Pt 1):1404–1410.
   PubMed Web of Science ®Google Scholar
• Moore CM, Brown S, Negrusz A, et al. Determination of cocaine and its major metabolite, benzoylecgonine, in amniotic fluid, umbilical cord blood, umbilical cord tissue, and neonatal urine: a case study. J Anal Toxicol. 1993;17(1):62.
   PubMed Web of Science ®Google Scholar
• Winecker RE, Goldberger BA, Tebbett I, et al. Detection of cocaine and its metabolites in amniotic fluid and umbilical cord tissue. J Anal Toxicol. 1997;21(2):97–104.
   PubMed Web of Science ®Google Scholar
• Ripple MG, Goldberger BA, Caplan YH, et al. Detection of cocaine and its metabolites in human amniotic fluid. J Anal Toxicol. 1992;16(5):328–331.
   PubMed Web of Science ®Google Scholar
• Srinivasan K, Wang PP, Eley AT, et al. Liquid chromatography--tandem mass spectrometry analysis of cocaine and its metabolites from blood, amniotic fluid, placental and fetal tissues: study of the metabolism and distribution of cocaine in pregnant rats. J Chromatogr B Biomed Sci Appl. 2000;745(2):287–303.
   PubMedGoogle Scholar
• Morishima HO, Whittington RA, Khan K, et al. Norcocaine: maternal to fetal transfer. Anesthesiology. 1996;85(3A):882.
   Web of Science ®Google Scholar
• Narkowicz S, Płotka J, Polkowska Ż, et al. Prenatal exposure to substance of abuse: a worldwide problem. Environ Int. 2013;54:141–163.
   PubMed Web of Science ®Google Scholar
• Hurt H, Betancourt LM, Malmud EK, et al. Children with and without gestational cocaine exposure: A neurocognitive systems analysis. Neurotoxicol Teratol. 2009;31:334–341.
   PubMed Web of Science ®Google Scholar
• Huang P, Kehner GB, Cowan A, et al. Comparison of pharmacological activities of buprenorphine and norbuprenorphine: norbuprenorphine is a potent opioid agonist. J Pharmacol Exp Ther. 2001;297(2):688–695.
   PubMed Web of Science ®Google Scholar
• Jansson LM, Velez M, McConnell K, et al. Maternal buprenorphine treatment and fetal neurobehavioral development. Am J Obstet Gynecol. 2017;216(5):529.
   PubMed Web of Science ®Google Scholar
• Chomchai S, Phuditshinnapatra J, Mekavuthikul P, et al. Effects of unconventional recreational drug use in pregnancy. J Matern Fetal Neonatal Med. 2019;24(2):1.
   Google Scholar
• Bondarev ML, Bondareva TS, Young R, et al. Behavioral and biochemical investigations of bupropion metabolites. Eur J Pharmacol. 2003;474:85–93.
   PubMed Web of Science ®Google Scholar
• Grabus SD, Carroll FI, Damaj MI. Bupropion and its main metabolite reverse nicotine chronic tolerance in the mouse. Nicotine Tob Res. 2012;14(11):1356–1361.
   PubMed Web of Science ®Google Scholar
• Ioakeimidis K, Vlachopoulos C, Katsi V, et al. Smoking cessation strategies in pregnancy: current concepts and controversies. Hellenic J Cardiol. 2019;60(1):11–15.
   PubMed Web of Science ®Google Scholar
• de Castro A, Jones HE, Johnson RE, et al. Maternal methadone dose, placental methadone concentrations, and neonatal outcomes. Clin Chem. 2011b;57(3):449–458.
   PubMed Web of Science ®Google Scholar
• Nekhayeva IA, Nanovskaya TN, Deshmukh SV, et al. Bidirectional transfer of methadone across human placenta. Biochem Pharmacol. 2005;69(1):187–197.
   PubMed Web of Science ®Google Scholar
• Sharpe C, Kuschel C. Outcomes of infants born to mothers receiving methadone for pain management in pregnancy. Arch Dis Child Fetal Neonatal Ed. 2004;89:33–36.
   PubMed Web of Science ®Google Scholar
• Bano U, Memon S, Shahani MY, et al. Epigenetic effects of in utero bisphenol A administration: diabetogenic and atherogenic changes in mice offspring. Iran J Basic Med Sci. 2019;22(5):521–528.
   PubMed Web of Science ®Google Scholar
• Matsumoto J, Yokota H, Yuasa A. Developmental increases in rat hepatic microsomal UDP glucuronosyltransferase activities toward xenoestrogens and decreases during pregnancy. Environ Health Perspect. 2002;110(2):193–196.
   PubMed Web of Science ®Google Scholar
• Strassburg CP, Strassburg A, Kneip S, et al. Developmental aspects of human hepatic drug glucuronidation in young children and adults. Gut. 2002;50(2):259–265.
   PubMed Web of Science ®Google Scholar
• Coughtrie MWH, Burchell B, Leakey JEA, et al. The inadequacy of perinatal glucuronidation: immunoblot analysis of the developmental expression of individual UDP-glucuronosyltransferase isoenzymes in rat and human liver microsomes. Mol Pharmacol. 1988;34(6):729–735.
   PubMed Web of Science ®Google Scholar
• Corbel T, Gayrard V, Puel S, et al. Bidirectional placental transfer of bisphenol A and its main metabolite, bisphenol A-glucuronide, in the isolated perfused human placenta. Reprod Toxicol. 2014;47:51–58.
   PubMed Web of Science ®Google Scholar
• Vom Saal FS, VandeVoort CA, Taylor JA, et al. Bisphenol A (BPA) pharmacokinetics with daily oral bolus or continuous exposure via silastic capsules in pregnant rhesus monkeys: relevance for human exposures. Reprod Toxicol. 2014;45:105–116.
   PubMed Web of Science ®Google Scholar
• Gauderat G, Picard-Hagen N, Toutain PL, et al. Bisphenol A glucuronide deconjugation is a determining factor of fetal exposure to bisphenol A. Environ Int. 2016;86:52–59.
   PubMed Web of Science ®Google Scholar
• Van de Bor M. Fetal toxicology. Handb Clin Neurol. 2019;162:31–55.
   PubMedGoogle Scholar
• Barrett ES, Sathyanarayana S, Mbowe O, et al. First-trimester urinary bisphenol a concentration in relation to anogenital distance, an androgen-sensitive measure of reproductive development, in infant girls. Environ Health Perspect. 2017;125(7):077008.
   PubMed Web of Science ®Google Scholar
• Mammadov E, Uncu M, Dalkan C. High prenatal exposure to bisphenol a reduces anogenital distance in healthy male newborns. J Clin Res Pediatr Endocrinol. 2018;10(1):25–29.
   PubMed Web of Science ®Google Scholar
• Lauer JM, Duggan CP, Ausman LM, et al. Maternal aflatoxin exposure during pregnancy and adverse birth outcomes in Uganda. Matern Child Nutr. 2019;15(2):e12701.
   PubMed Web of Science ®Google Scholar
• Wild CP, Rasheed FN, Jawla MF, et al. In-utero exposure to aflatoxin in west Africa. Lancet. 1991;337(8757):1602.
   PubMed Web of Science ®Google Scholar
• Hsieh LL, Hsieh TT. Detection of aflatoxin B1-DNA adducts in human placenta and cord blood. Cancer Res. 1993;53(6):1278–1280.
   PubMed Web of Science ®Google Scholar
• Turner PC, Collinson AC, Cheung YB, et al. Aflatoxin exposure in utero causes growth faltering in Gambian infants. Int J Epidemiol. 2007;36:1119–1125.
   PubMed Web of Science ®Google Scholar
• Joseph P, Srinivasan SN, Byczkowski JZ, et al. Bioactivation of benzo(a)pyrene-7,8-dihydrodiol catalyzed by lipoxygenase purified from human term placenta and conceptal tissues. Reprod Toxicol. 1994;8(4):307–313.
   PubMed Web of Science ®Google Scholar
• Phillips DH. Smoking-related DNA and protein adducts in human tissues. Carcinogenesis. 2002;23:1979–2004.
   PubMed Web of Science ®Google Scholar
• Perera FP, Rauh V, Whyatt RM, et al. A summary of recent findings on birth outcomes and developmental effects of prenatal ETS, PAH, and pesticide exposures. Neurotoxicology. 2005;26(4):573–587.
   PubMed Web of Science ®Google Scholar
• Wang S, Chanock S, Tang D, et al. Assessment of interactions between PAH exposure and genetic polymorphisms on PAH–DNA adducts in African, American, Dominican, and Caucasian mothers and newborns. Cancer Epidemiol Biomarkers Prev. 2008;17:405–413.
   PubMed Web of Science ®Google Scholar
• Dejmek J, Solanský I, Benes I, et al. The impact of polycyclic aromatic hydrocarbons and fine particles on pregnancy outcome. Environ Health Perspect. 2000;108(12):1159–1164.
   PubMed Web of Science ®Google Scholar
• Perera FP, Rauh V, Tsai WY, et al. Effects of transplacental exposure to environmental pollutants on birth outcomes in a multiethnic population. Environ Health Perspect. 2003;111(2):201–205.
   PubMed Web of Science ®Google Scholar
• Detmar J, Rennie MY, Whiteley KJ, et al. Fetal growth restriction triggered by polycyclic aromatic hydrocarbons is associated with altered placental vasculature and AhR-dependent changes in cell death. Am J Physiol Endocrinol Metab. 2008;295:519–530.
   Web of Science ®Google Scholar