Semin Reprod Med 2017; 35(03): 205-216
DOI: 10.1055/s-0037-1603570
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Abnormal Placentation Associated with Infertility as a Marker of Overall Health

Lauren W. Sundheimer
1   Department of Obstetrics and Gynecology, Cedars-Sinai Medical Center, Los Angeles, California
2   Division of Reproductive Endocrinology and Infertility, UCLA David Geffen School of Medicine, Los Angeles, California
,
Margareta D. Pisarska
1   Department of Obstetrics and Gynecology, Cedars-Sinai Medical Center, Los Angeles, California
2   Division of Reproductive Endocrinology and Infertility, UCLA David Geffen School of Medicine, Los Angeles, California
› Author Affiliations
Further Information

Publication History

Publication Date:
28 June 2017 (online)

Abstract

Infertility and fertility treatments utilized are associated with abnormal placentation leading to adverse pregnancy outcomes related to placentation, including preterm birth, low birth weight, placenta accrete, and placenta previa. This may be due to the underlying genetics predisposing to infertility or the epigenetic changes associated with the fertility treatments utilized, as specific disease states leading to infertility are at increased risk of adverse outcomes, including placental abruption, fetal loss, gestational diabetes mellitus, and outcomes related to placentation, as well as the treatments utilized including in vitro fertilization (IVF) and non-IVF fertility treatment. Placentation defects, leading to adverse maternal and fetal outcomes, which are more pronounced in the infertile population, occur due to changes in trophoblast invasion, vascular defects, changes in the environmental milieu, chronic inflammation, and oxidative stress. These similar processes are recognized as major contributors to lifelong risk of cardiovascular and metabolic disease for both the mother and her offspring. Thus, abnormal placentation, found to be more prevalent in the infertile population, may be the key to better understand how infertility affects overall and long-term health.

 
  • References

  • 1 Messerlian C, Maclagan L, Basso O. Infertility and the risk of adverse pregnancy outcomes: a systematic review and meta-analysis. Hum Reprod 2013; 28 (01) 125-137
  • 2 Jauniaux E, Jurkovic D. Placenta accreta: pathogenesis of a 20th century iatrogenic uterine disease. Placenta 2012; 33 (04) 244-251
  • 3 Healy DL, Breheny S, Halliday J. , et al. Prevalence and risk factors for obstetric haemorrhage in 6730 singleton births after assisted reproductive technology in Victoria Australia. Hum Reprod 2010; 25 (01) 265-274
  • 4 Takemura Y, Osuga Y, Fujimoto A. , et al. Increased risk of placenta previa is associated with endometriosis and tubal factor infertility in assisted reproductive technology pregnancy. Gynecol Endocrinol 2013; 29 (02) 113-115
  • 5 Igarashi TM, Bruner-Tran KL, Yeaman GR. , et al. Reduced expression of progesterone receptor-B in the endometrium of women with endometriosis and in cocultures of endometrial cells exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fertil Steril 2005; 84 (01) 67-74
  • 6 Podgaec S, Abrao MS, Dias Jr JA, Rizzo LV, de Oliveira RM, Baracat EC. Endometriosis: an inflammatory disease with a Th2 immune response component. Hum Reprod 2007; 22 (05) 1373-1379
  • 7 Boomsma CM, Eijkemans MJ, Hughes EG, Visser GH, Fauser BC, Macklon NS. A meta-analysis of pregnancy outcomes in women with polycystic ovary syndrome. Hum Reprod Update 2006; 12 (06) 673-683
  • 8 Kjerulff LE, Sanchez-Ramos L, Duffy D. Pregnancy outcomes in women with polycystic ovary syndrome: a metaanalysis. Am J Obstet Gynecol 2011; 204 (06) 558.e1-558.e6
  • 9 Qin JZ, Pang LH, Li MJ, Fan XJ, Huang RD, Chen HY. Obstetric complications in women with polycystic ovary syndrome: a systematic review and meta-analysis. Reprod Biol Endocrinol 2013; 11 (56) 56
  • 10 Palomba S, de Wilde MA, Falbo A, Koster MP, La Sala GB, Fauser BC. Pregnancy complications in women with polycystic ovary syndrome. Hum Reprod Update 2015; 21 (05) 575-592
  • 11 Vambergue A, Fajardy I. Consequences of gestational and pregestational diabetes on placental function and birth weight. World J Diabetes 2011; 2 (11) 196-203
  • 12 Madsen H, Ditzel J. Blood-oxygen transport in first trimester of diabetic pregnancy. Acta Obstet Gynecol Scand 1984; 63 (04) 317-320
  • 13 Baptiste-Roberts K, Salafia CM, Nicholson WK, Duggan A, Wang NY, Brancati FL. Maternal risk factors for abnormal placental growth: the national collaborative perinatal project. BMC Pregnancy Childbirth 2008; 8: 44
  • 14 Klemetti R, Gissler M, Sevón T, Koivurova S, Ritvanen A, Hemminki E. Children born after assisted fertilization have an increased rate of major congenital anomalies. Fertil Steril 2005; 84 (05) 1300-1307
  • 15 Shevell T, Malone FD, Vidaver J. , et al. Assisted reproductive technology and pregnancy outcome. Obstet Gynecol 2005; 106 (5, Pt 1): 1039-1045
  • 16 Jackson RA, Gibson KA, Wu YW, Croughan MS. Perinatal outcomes in singletons following in vitro fertilization: a meta-analysis. Obstet Gynecol 2004; 103 (03) 551-563
  • 17 Rimm AA, Katayama AC, Diaz M, Katayama KP. A meta-analysis of controlled studies comparing major malformation rates in IVF and ICSI infants with naturally conceived children. J Assist Reprod Genet 2004; 21 (12) 437-443
  • 18 Hansen M, Kurinczuk JJ, Bower C, Webb S. The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N Engl J Med 2002; 346 (10) 725-730
  • 19 Strömberg B, Dahlquist G, Ericson A, Finnström O, Köster M, Stjernqvist K. Neurological sequelae in children born after in-vitro fertilisation: a population-based study. Lancet 2002; 359 (9305): 461-465
  • 20 Schieve LA, Meikle SF, Ferre C, Peterson HB, Jeng G, Wilcox LS. Low and very low birth weight in infants conceived with use of assisted reproductive technology. N Engl J Med 2002; 346 (10) 731-737
  • 21 Verlaenen H, Cammu H, Derde MP, Amy JJ. Singleton pregnancy after in vitro fertilization: expectations and outcome. Obstet Gynecol 1995; 86 (06) 906-910
  • 22 Kroener L, Wang ET, Pisarska MD. Predisposing factors to abnormal first trimester placentation and the impact on fetal outcomes. Semin Reprod Med 2016; 34 (01) 27-35
  • 23 Moser G, Weiss G, Sundl M. , et al. Extravillous trophoblasts invade more than uterine arteries: evidence for the invasion of uterine veins. Histochem Cell Biol 2017; 147 (03) 353-366
  • 24 Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 2006; 27 (9-10): 939-958
  • 25 Brosens I, Robertson WB, Dixon HG. The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol 1967; 93 (02) 569-579
  • 26 Whitley GS, Cartwright JE. Cellular and molecular regulation of spiral artery remodelling: lessons from the cardiovascular field. Placenta 2010; 31 (06) 465-474
  • 27 Zhou Y, Fisher SJ, Janatpour M. , et al. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?. J Clin Invest 1997; 99 (09) 2139-2151
  • 28 Cao TC, Thirkill TL, Wells M, Barakat AI, Douglas GC. Trophoblasts and shear stress induce an asymmetric distribution of icam-1 in uterine endothelial cells. Am J Reprod Immunol 2008; 59 (02) 167-181
  • 29 Soghomonians A, Barakat AI, Thirkill TL, Douglas GC. Trophoblast migration under flow is regulated by endothelial cells. Biol Reprod 2005; 73 (01) 14-19
  • 30 Roberts CT. IFPA Award in Placentology Lecture: complicated interactions between genes and the environment in placentation, pregnancy outcome and long term health. Placenta 2010; 31 (Suppl): S47-S53
  • 31 Burton GJ, Woods AW, Jauniaux E, Kingdom JC. Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 2009; 30 (06) 473-482
  • 32 Brosens IA. ; IA. Morphological changes in the utero-placental bed in pregnancy hypertension. Clin Obstet Gynaecol 1977; 4 (03) 573-593
  • 33 Miwa I, Sase M, Torii M, Sanai H, Nakamura Y, Ueda K. A thick placenta: a predictor of adverse pregnancy outcomes. Springerplus 2014; 3: 353
  • 34 Raio L, Ghezzi F, Cromi A, Nelle M, Dürig P, Schneider H. The thick heterogeneous (jellylike) placenta: a strong predictor of adverse pregnancy outcome. Prenat Diagn 2004; 24 (03) 182-188
  • 35 de Waal E, Vrooman LA, Fischer E. , et al. The cumulative effect of assisted reproduction procedures on placental development and epigenetic perturbations in a mouse model. Hum Mol Genet 2015; 24 (24) 6975-6985
  • 36 Churchill S, Wang EW, Goldstein EH. , et al. Mode of conception does not appear to affect placental volume in the first trimester. Fertil Steril 2017; 107 (06) 1341-1347
  • 37 Balayla J, Bondarenko HD. Placenta accreta and the risk of adverse maternal and neonatal outcomes. J Perinat Med 2013; 41 (02) 141-149
  • 38 Dommisse J, Tiltman AJ. Placental bed biopsies in placental abruption. Br J Obstet Gynaecol 1992; 99 (08) 651-654
  • 39 Salafia CM, López-Zeno JA, Sherer DM, Whittington SS, Minior VK, Vintzileos AM. Histologic evidence of old intrauterine bleeding is more frequent in prematurity. Am J Obstet Gynecol 1995; 173 (04) 1065-1070
  • 40 Rayne SC, Kraus FT. Placental thrombi and other vascular lesions. Classification, morphology, and clinical correlations. Pathol Res Pract 1993; 189 (01) 2-17
  • 41 Eskes TK. Clotting disorders and placental abruption: homocysteine--a new risk factor. Eur J Obstet Gynecol Reprod Biol 2001; 95 (02) 206-212
  • 42 Redman CW. Preeclampsia: a multi-stress disorder. Rev Med Interne 2011; 32 (Suppl. 01) S41-S44
  • 43 Roberts JM, Hubel CA. The two stage model of preeclampsia: variations on the theme. Placenta 2009; 30 (Suppl A): S32-S37
  • 44 Brosens I, Pijnenborg R, Vercruysse L, Romero R. The “Great Obstetrical Syndromes” are associated with disorders of deep placentation. Am J Obstet Gynecol 2011; 204 (03) 193-201
  • 45 Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of pre-eclampsia. J Pathol 1970 ;101(04)
  • 46 Fisher SJ. ; SJ. Why is placentation abnormal in preeclampsia?. Am J Obstet Gynecol 2015; 213 (4, Suppl): S115-S122
  • 47 Schipper EJ, Bolte AC, Schalkwijk CG, Van Geijn HP, Dekker GA. TNF-receptor levels in preeclampsia--results of a longitudinal study in high-risk women. J Matern Fetal Neonatal Med 2005; 18 (05) 283-287
  • 48 Maynard SE, Venkatesha S, Thadhani R, Karumanchi SA. Soluble Fms-like tyrosine kinase 1 and endothelial dysfunction in the pathogenesis of preeclampsia. Pediatr Res 2005; 57 (5, Pt 2): 1R-7R
  • 49 Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science 2005; 308 (5728): 1592-1594
  • 50 Brosens IA, Robertson WB, Dixon HG. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1972; 1: 177-191
  • 51 Burton GJ, Yung HW, Cindrova-Davies T, Charnock-Jones DS. Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 2009; 30 (Suppl A): S43-S48
  • 52 Abumaree MH, Stone PR, Chamley LW. The effects of apoptotic, deported human placental trophoblast on macrophages: possible consequences for pregnancy. J Reprod Immunol 2006; 72 (1-2): 33-45
  • 53 Powe CE, Levine RJ, Karumanchi SA. Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease. Circulation 2011; 123 (24) 2856-2869
  • 54 Mutter WP, Karumanchi SA. Molecular mechanisms of preeclampsia. Microvasc Res 2008; 75 (01) 1-8
  • 55 Poston L, McCarthy AL, Ritter JM. Control of vascular resistance in the maternal and feto-placental arterial beds. Pharmacol Ther 1995; 65 (02) 215-239
  • 56 Suzuki Y, Hattori T, Kajikuri J, Yamamoto T, Suzumori K, Itoh T. Reduced function of endothelial prostacyclin in human omental resistance arteries in pre-eclampsia. J Physiol 2002; 545 (Pt 1): 269-277
  • 57 Mahdy Z, Otun HA, Dunlop W, Gillespie JI. The responsiveness of isolated human hand vein endothelial cells in normal pregnancy and in pre-eclampsia. J Physiol 1998; 508 (Pt 2): 609-617
  • 58 Levine RJ, Maynard SE, Qian C. , et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350 (07) 672-683
  • 59 Venkatesha S, Toporsian M, Lam C. , et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006; 12 (06) 642-649
  • 60 Levine RJ, Lam C, Qian C. , et al; CPEP Study Group. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006; 355 (10) 992-1005
  • 61 Cartwright JE, Fraser R, Leslie K, Wallace AE, James JL. Remodelling at the maternal-fetal interface: relevance to human pregnancy disorders. Reproduction 2010; 140 (06) 803-813
  • 62 Hendricks SK, Sorensen TK, Wang KY, Bushnell JM, Seguin EM, Zingheim RW. Doppler umbilical artery waveform indices--normal values from fourteen to forty-two weeks. Am J Obstet Gynecol 1989; 161 (03) 761-765
  • 63 Jackson MR, Walsh AJ, Morrow RJ, Mullen JB, Lye SJ, Ritchie JW. Reduced placental villous tree elaboration in small-for-gestational-age pregnancies: relationship with umbilical artery Doppler waveforms. Am J Obstet Gynecol 1995; 172 (2, Pt 1): 518-525
  • 64 Burton GJ, Jauniaux E, Charnock-Jones DS. The influence of the intrauterine environment on human placental development. Int J Dev Biol 2010; 54 (2-3): 303-312
  • 65 Campbell S, Pearce JM, Hackett G, Cohen-Overbeek T, Hernandez C. Qualitative assessment of uteroplacental blood flow: early screening test for high-risk pregnancies. Obstet Gynecol 1986; 68 (05) 649-653
  • 66 Papageorghiou AT, Yu CK, Bindra R, Pandis G, Nicolaides KH. ; Fetal Medicine Foundation Second Trimester Screening Group. Multicenter screening for pre-eclampsia and fetal growth restriction by transvaginal uterine artery Doppler at 23 weeks of gestation. Ultrasound Obstet Gynecol 2001; 18 (05) 441-449
  • 67 Harrington K, Goldfrad C, Carpenter RG, Campbell S. Transvaginal uterine and umbilical artery Doppler examination of 12-16 weeks and the subsequent development of pre-eclampsia and intrauterine growth retardation. Ultrasound Obstet Gynecol 1997; 9 (02) 94-100
  • 68 Hafner E, Schuchter K, van Leeuwen M, Metzenbauer M, Dillinger-Paller B, Philipp K. Three-dimensional sonographic volumetry of the placenta and the fetus between weeks 15 and 17 of gestation. Ultrasound Obstet Gynecol 2001; 18 (02) 116-120
  • 69 Hafner E, Philipp T, Schuchter K, Dillinger-Paller B, Philipp K, Bauer P. Second-trimester measurements of placental volume by three-dimensional ultrasound to predict small-for-gestational-age infants. Ultrasound Obstet Gynecol 1998; 12 (02) 97-102
  • 70 Metzenbauer M, Hafner E, Hoefinger D. , et al. Three-dimensional ultrasound measurement of the placental volume in early pregnancy: method and correlation with biochemical placenta parameters. Placenta 2001; 22 (06) 602-605
  • 71 Schuchter K, Metzenbauer M, Hafner E, Philipp K. Uterine artery Doppler and placental volume in the first trimester in the prediction of pregnancy complications. Ultrasound Obstet Gynecol 2001; 18 (06) 590-592
  • 72 Romero R, Dey SK, Fisher SJ. Preterm labor: one syndrome, many causes. Science 2014; 345 (6198): 760-765
  • 73 Kim YM, Bujold E, Chaiworapongsa T. , et al. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2003; 189 (04) 1063-1069
  • 74 Lee B, Kroener LL, Xu N. , et al. Function and hormonal regulation of GATA3 in human first trimester placentation. Biol Reprod 2016; 95 (05) 113
  • 75 Wang ET, Ozimek JA, Greene N. , et al. Impact of fertility treatment on severe maternal morbidity. Fertil Steril 2016; 106 (02) 423-426
  • 76 Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig 2004; 11 (06) 342-352
  • 77 Hempstock J, Jauniaux E, Greenwold N, Burton GJ. The contribution of placental oxidative stress to early pregnancy failure. Hum Pathol 2003; 34 (12) 1265-1275
  • 78 Brosens IA, Fusi L, Brosens JJ. Endometriosis is a risk factor for spontaneous hemoperitoneum during pregnancy. Fertil Steril 2009; 92 (04) 1243-1245
  • 79 Brosens I, Brosens JJ, Fusi L, Al-Sabbagh M, Kuroda K, Benagiano G. Risks of adverse pregnancy outcome in endometriosis. Fertil Steril 2012; 98 (01) 30-35
  • 80 Petraglia F, Arcuri F, de Ziegler D, Chapron C. Inflammation: a link between endometriosis and preterm birth. Fertil Steril 2012; 98 (01) 36-40
  • 81 Viganò P, Somigliana E, Panina P, Rabellotti E, Vercellini P, Candiani M. Principles of phenomics in endometriosis. Hum Reprod Update 2012; 18 (03) 248-259
  • 82 Barbosa MA, Teixeira DM, Navarro PA, Ferriani RA, Nastri CO, Martins WP. Impact of endometriosis and its staging on assisted reproduction outcome: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2014; 44 (03) 261-278
  • 83 Leone Roberti Maggiore U, Ferrero S, Mangili G. , et al. A systematic review on endometriosis during pregnancy: diagnosis, misdiagnosis, complications and outcomes. Hum Reprod Update 2016; 22 (01) 70-103
  • 84 Roos N, Kieler H, Sahlin L, Ekman-Ordeberg G, Falconer H, Stephansson O. Risk of adverse pregnancy outcomes in women with polycystic ovary syndrome: population based cohort study. BMJ 2011; 343: d6309
  • 85 Jindal P, Regan L, Fourkala EO. , et al. Placental pathology of recurrent spontaneous abortion: the role of histopathological examination of products of conception in routine clinical practice: a mini review. Hum Reprod 2007; 22 (02) 313-316
  • 86 Longtine MS, Nelson DM. Placental dysfunction and fetal programming: the importance of placental size, shape, histopathology, and molecular composition. Semin Reprod Med 2011; 29 (03) 187-196
  • 87 Palomba S, Russo T, Falbo A. , et al. Macroscopic and microscopic findings of the placenta in women with polycystic ovary syndrome. Hum Reprod 2013; 28 (10) 2838-2847
  • 88 Palomba S, Falbo A, Chiossi G. , et al. Early trophoblast invasion and placentation in women with different PCOS phenotypes. Reprod Biomed Online 2014; 29 (03) 370-381
  • 89 Palomba S, Russo T, Falbo A. , et al. Decidual endovascular trophoblast invasion in women with polycystic ovary syndrome: an experimental case-control study. J Clin Endocrinol Metab 2012; 97 (07) 2441-2449
  • 90 Palomba S, Santagni S, Falbo A, La Sala GB. Complications and challenges associated with polycystic ovary syndrome: current perspectives. Int J Womens Health 2015; 7: 745-763
  • 91 Palomba S, Falbo A, Russo T. , et al. Uterine blood flow in pregnant patients with polycystic ovary syndrome: relationships with clinical outcomes. BJOG 2010; 117 (06) 711-721
  • 92 Maccani MA, Marsit CJ. Epigenetics in the placenta. Am J Reprod Immunol 2009; 62 (02) 78-89
  • 93 Robins JC, Marsit CJ, Padbury JF, Sharma SS. Endocrine disruptors, environmental oxygen, epigenetics and pregnancy. Front Biosci (Elite Ed) 2011; 3: 690-700
  • 94 Novakovic B, Rakyan V, Ng HK. , et al. Specific tumour-associated methylation in normal human term placenta and first-trimester cytotrophoblasts. Mol Hum Reprod 2008; 14 (09) 547-554
  • 95 Santos F, Hendrich B, Reik W, Dean W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 2002; 241 (01) 172-182
  • 96 Rahnama F, Shafiei F, Gluckman PD, Mitchell MD, Lobie PE. Epigenetic regulation of human trophoblastic cell migration and invasion. Endocrinology 2006; 147 (11) 5275-5283
  • 97 Jones ML, Mark PJ, Mori TA, Keelan JA, Waddell BJ. Maternal dietary omega-3 fatty acid supplementation reduces placental oxidative stress and increases fetal and placental growth in the rat. Biol Reprod 2013; 88 (02) 37
  • 98 Roberts VH, Smith J, McLea SA, Heizer AB, Richardson JL, Myatt L. Effect of increasing maternal body mass index on oxidative and nitrative stress in the human placenta. Placenta 2009; 30 (02) 169-175
  • 99 Myatt L. Review: Reactive oxygen and nitrogen species and functional adaptation of the placenta. Placenta 2010; 31 (Suppl): S66-S69
  • 100 Yang X, Guo L, Li H, Chen X, Tong X. Analysis of the original causes of placental oxidative stress in normal pregnancy and pre-eclampsia: a hypothesis. J Matern Fetal Neonatal Med 2012; 25 (07) 884-888
  • 101 Xu N, Barlow GM, Cui J. , et al. Comparison of genome-wide and gene-specific DNA methylation profiling in first trimester chorionic villi from pregnancies conceived with infertility treatments. Reprod Sci 2016; 1-9 . DOI:1933719116675056
  • 102 Martin AS, Monsour M, Kissin DM, Jamieson DJ, Callaghan WM, Boulet SL. Trends in severe maternal morbidity after assisted reproductive technology in the United States, 2008-2012. Obstet Gynecol 2016; 127 (01) 59-66
  • 103 Katari S, Turan N, Bibikova M. , et al. DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet 2009; 18 (20) 3769-3778
  • 104 Turan N, Ghalwash MF, Katari S, Coutifaris C, Obradovic Z, Sapienza C. DNA methylation differences at growth related genes correlate with birth weight: a molecular signature linked to developmental origins of adult disease?. BMC Med Genomics 2012; 5: 10
  • 105 Melamed N, Choufani S, Wilkins-Haug LE, Koren G, Weksberg R. Comparison of genome-wide and gene-specific DNA methylation between ART and naturally conceived pregnancies. Epigenetics 2015; 10 (06) 474-483
  • 106 Nelissen EC, van Montfoort AP, Dumoulin JC, Evers JL. Epigenetics and the placenta. Hum Reprod Update 2011; 17 (03) 397-417
  • 107 Wale PL, Gardner DK. The effects of chemical and physical factors on mammalian embryo culture and their importance for the practice of assisted human reproduction. Hum Reprod Update 2016; 22 (01) 2-22
  • 108 Song S, Ghosh J, Mainigi M. , et al. DNA methylation differences between in vitro- and in vivo-conceived children are associated with ART procedures rather than infertility. Clin Epigenetics 2015; 7 (01) 41
  • 109 Shi W, Haaf T. Aberrant methylation patterns at the two-cell stage as an indicator of early developmental failure. Mol Reprod Dev 2002; 63 (03) 329-334
  • 110 Chen JZ, Sheehan PM, Brennecke SP, Keogh RJ. Vessel remodelling, pregnancy hormones and extravillous trophoblast function. Mol Cell Endocrinol 2012; 349 (02) 138-144
  • 111 Imudia AN, Awonuga AO, Doyle JO. , et al. Peak serum estradiol level during controlled ovarian hyperstimulation is associated with increased risk of small for gestational age and preeclampsia in singleton pregnancies after in vitro fertilization. Fertil Steril 2012; 97 (06) 1374-1379
  • 112 Joy J, Gannon C, McClure N, Cooke I. Is assisted reproduction associated with abnormal placentation?. Pediatr Dev Pathol 2012; 15 (04) 306-314
  • 113 Jauniaux E, Englert Y, Vanesse M, Hiden M, Wilkin P. Pathologic features of placentas from singleton pregnancies obtained by in vitro fertilization and embryo transfer. Obstet Gynecol 1990; 76 (01) 61-64
  • 114 Daniel Y, Schreiber L, Geva E. , et al. Do placentae of term singleton pregnancies obtained by assisted reproductive technologies differ from those of spontaneously conceived pregnancies?. Hum Reprod 1999; 14 (04) 1107-1110
  • 115 Zhang Y, Zhao W, Jiang Y. , et al. Ultrastructural study on human placentae from women subjected to assisted reproductive technology treatments. Biol Reprod 2011; 85 (03) 635-642
  • 116 Männistö T, Mendola P, Vääräsmäki M. , et al. Elevated blood pressure in pregnancy and subsequent chronic disease risk. Circulation 2013; 127 (06) 681-690
  • 117 Libby G, Murphy DJ, McEwan NF. , et al; DARTS/MEMO Collaboration. Pre-eclampsia and the later development of type 2 diabetes in mothers and their children: an intergenerational study from the Walker cohort. Diabetologia 2007; 50 (03) 523-530
  • 118 Brown MC, Best KE, Pearce MS, Waugh J, Robson SC, Bell R. Cardiovascular disease risk in women with pre-eclampsia: systematic review and meta-analysis. Eur J Epidemiol 2013; 28 (01) 1-19
  • 119 Kvehaugen AS, Dechend R, Ramstad HB, Troisi R, Fugelseth D, Staff AC. Endothelial function and circulating biomarkers are disturbed in women and children after preeclampsia. Hypertension 2011; 58 (01) 63-69
  • 120 Davis EF, Lazdam M, Lewandowski AJ. , et al. Cardiovascular risk factors in children and young adults born to preeclamptic pregnancies: a systematic review. Pediatrics 2012; 129 (06) e1552-e1561
  • 121 Thoulass JC, Robertson L, Denadai L. , et al. Hypertensive disorders of pregnancy and adult offspring cardiometabolic outcomes: a systematic review of the literature and meta-analysis. J Epidemiol Community Health 2016; 70 (04) 414-422
  • 122 Miettola S, Hartikainen AL, Vääräsmäki M. , et al. Offspring's blood pressure and metabolic phenotype after exposure to gestational hypertension in utero. Eur J Epidemiol 2013; 28 (01) 87-98
  • 123 Kajantie E, Eriksson JG, Osmond C, Thornburg K, Barker DJ. Pre-eclampsia is associated with increased risk of stroke in the adult offspring: the Helsinki birth cohort study. Stroke 2009; 40 (04) 1176-1180
  • 124 van Vliet EO, de Kieviet JF, van der Voorn JP, Been JV, Oosterlaan J, van Elburg RM. Placental pathology and long-term neurodevelopment of very preterm infants. Am J Obstet Gynecol 2012; 206 (06) 489.e1-489.e7
  • 125 Whitehouse AJ, Robinson M, Newnham JP, Pennell CE. Do hypertensive diseases of pregnancy disrupt neurocognitive development in offspring?. Paediatr Perinat Epidemiol 2012; 26 (02) 101-108
  • 126 He J, Zhang A, Fang M. , et al. Methylation levels at IGF2 and GNAS DMRs in infants born to preeclamptic pregnancies. BMC Genomics 2013; 14: 472
  • 127 Rexhaj E, Paoloni-Giacobino A, Rimoldi SF. , et al. Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span. J Clin Invest 2013; 123 (12) 5052-5060
  • 128 Jayet PY, Rimoldi SF, Stuber T. , et al. Pulmonary and systemic vascular dysfunction in young offspring of mothers with preeclampsia. Circulation 2010; 122 (05) 488-494
  • 129 Rimoldi SF, Sartori C, Rexhaj E. , et al. Antioxidants improve vascular function in children conceived by assisted reproductive technologies: a randomized double-blind placebo-controlled trial. Eur J Prev Cardiol 2015; 22 (11) 1399-1407
  • 130 Watkins AJ, Platt D, Papenbrock T. , et al. Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure. Proc Natl Acad Sci U S A 2007; 104 (13) 5449-5454
  • 131 Callaghan WM, Creanga AA, Kuklina EV. Severe maternal morbidity among delivery and postpartum hospitalizations in the United States. Obstet Gynecol 2012; 120 (05) 1029-1036
  • 132 Cunningham FG, Leveno KJ. Childbearing among older women--the message is cautiously optimistic. N Engl J Med 1995; 333 (15) 1002-1004
  • 133 Kenny LC, Lavender T, McNamee R, O'Neill SM, Mills T, Khashan AS. Advanced maternal age and adverse pregnancy outcome: evidence from a large contemporary cohort. PLoS One 2013; 8 (02) e56583
  • 134 Jackson S, Hong C, Wang ET, Alexander C, Gregory KD, Pisarska MD. Pregnancy outcomes in very advanced maternal age pregnancies: the impact of assisted reproductive technology. Fertil Steril 2015; 103 (01) 76-80
  • 135 Wang IK, Muo CH, Chang YC. , et al. Association between hypertensive disorders during pregnancy and end-stage renal disease: a population-based study. CMAJ 2013; 185 (03) 207-213
  • 136 Vikse BE, Irgens LM, Leivestad T, Skjaerven R, Iversen BM. Preeclampsia and the risk of end-stage renal disease. N Engl J Med 2008; 359 (08) 800-809
  • 137 Levine RJ, Vatten LJ, Horowitz GL. , et al. Pre-eclampsia, soluble fms-like tyrosine kinase 1, and the risk of reduced thyroid function: nested case-control and population based study. BMJ 2009; 339: b4336
  • 138 Wilson KL, Casey BM, McIntire DD, Halvorson LM, Cunningham FG. Subclinical thyroid disease and the incidence of hypertension in pregnancy. Obstet Gynecol 2012; 119 (2, Pt 1): 315-320
  • 139 Sara JD, Zhang M, Gharib H, Lerman LO, Lerman A. Hypothyroidism is associated with coronary endothelial dysfunction in women. J Am Heart Assoc 2015; 4 (08) e002225
  • 140 Mosca L, Benjamin EJ, Berra K. , et al; American Heart Association. Effectiveness-based guidelines for the prevention of cardiovascular disease in women--2011 update: a guideline from the American Heart Association. J Am Coll Cardiol 2011; 57 (12) 1404-1423
  • 141 Bellamy L, Casas JP, Hingorani AD, Williams DJ. Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ 2007; 335 (7627): 974
  • 142 Heida KY, Franx A, van Rijn BB. , et al. Earlier age of onset of chronic hypertension and type 2 diabetes mellitus after a hypertensive disorder of pregnancy or gestational diabetes mellitus. Hypertension 2015; 66 (06) 1116-1122
  • 143 Mongraw-Chaffin ML, Cirillo PM, Cohn BA. Preeclampsia and cardiovascular disease death: prospective evidence from the child health and development studies cohort. Hypertension 2010; 56 (01) 166-171
  • 144 Chambers JC, Fusi L, Malik IS, Haskard DO, De Swiet M, Kooner JS. Association of maternal endothelial dysfunction with preeclampsia. JAMA 2001; 285 (12) 1607-1612
  • 145 Agatisa PK, Ness RB, Roberts JM, Costantino JP, Kuller LH, McLaughlin MK. Impairment of endothelial function in women with a history of preeclampsia: an indicator of cardiovascular risk. Am J Physiol Heart Circ Physiol 2004; 286 (04) H1389-H1393
  • 146 Lampinen KH, Rönnback M, Kaaja RJ, Groop PH. Impaired vascular dilatation in women with a history of pre-eclampsia. J Hypertens 2006; 24 (04) 751-756
  • 147 Yinon Y, Kingdom JC, Odutayo A. , et al. Vascular dysfunction in women with a history of preeclampsia and intrauterine growth restriction: insights into future vascular risk. Circulation 2010; 122 (18) 1846-1853
  • 148 Hermes W, Ket JC, van Pampus MG. , et al. Biochemical cardiovascular risk factors after hypertensive pregnancy disorders: a systematic review and meta-analysis. Obstet Gynecol Surv 2012; 67 (12) 793-809
  • 149 Magnussen EB, Vatten LJ, Lund-Nilsen TI, Salvesen KA, Davey Smith G, Romundstad PR. Prepregnancy cardiovascular risk factors as predictors of pre-eclampsia: population based cohort study. BMJ 2007; 335 (7627): 978
  • 150 Magnussen EB, Vatten LJ, Smith GD, Romundstad PR. Hypertensive disorders in pregnancy and subsequently measured cardiovascular risk factors. Obstet Gynecol 2009; 114 (05) 961-970
  • 151 Romundstad PR, Magnussen EB, Smith GD, Vatten LJ. Hypertension in pregnancy and later cardiovascular risk: common antecedents?. Circulation 2010; 122 (06) 579-584
  • 152 Bytautiene E, Bulayeva N, Bhat G, Li L, Rosenblatt KP, Saade GR. Long-term alterations in maternal plasma proteome after sFlt1-induced preeclampsia in mice. Am J Obstet Gynecol 2013; 208 (05) 388.e1-388.e10
  • 153 Tomiyama H, Yamashina A. Non-invasive vascular function tests: their pathophysiological background and clinical application. Circ J 2010; 74 (01) 24-33
  • 154 Green DJ, Jones H, Thijssen D, Cable NT, Atkinson G. Flow-mediated dilation and cardiovascular event prediction: does nitric oxide matter?. Hypertension 2011; 57 (03) 363-369
  • 155 Ras RT, Streppel MT, Draijer R, Zock PL. Flow-mediated dilation and cardiovascular risk prediction: a systematic review with meta-analysis. Int J Cardiol 2013; 168 (01) 344-351
  • 156 Dørup I, Skajaa K, Sørensen KE. Normal pregnancy is associated with enhanced endothelium-dependent flow-mediated vasodilation. Am J Physiol 1999; 276 (3, Pt 2): H821-H825
  • 157 Weissgerber TL, Milic NM, Milin-Lazovic JS, Garovic VD. Impaired flow-mediated dilation before, during, and after preeclampsia: a systematic review and meta-analysis. Hypertension 2016; 67 (02) 415-423
  • 158 Kessous R, Shoham-Vardi I, Pariente G, Sherf M, Sheiner E. An association between gestational diabetes mellitus and long-term maternal cardiovascular morbidity. Heart 2013; 99 (15) 1118-1121
  • 159 Smith GD, Whitley E, Gissler M, Hemminki E. Birth dimensions of offspring, premature birth, and the mortality of mothers. Lancet 2000; 356 (9247): 2066-2067
  • 160 Kaaja RJ, Pöyhönen-Alho MK. Insulin resistance and sympathetic overactivity in women. J Hypertens 2006; 24 (01) 131-141
  • 161 Kaaja RJ, Greer IA. Manifestations of chronic disease during pregnancy. JAMA 2005; 294 (21) 2751-2757
  • 162 Stekkinger E, Zandstra M, Peeters LL, Spaanderman ME. Early-onset preeclampsia and the prevalence of postpartum metabolic syndrome. Obstet Gynecol 2009; 114 (05) 1076-1084
  • 163 Zandstra M, Stekkinger E, van der Vlugt MJ, van Dijk AP, Lotgering FK, Spaanderman ME. Cardiac diastolic dysfunction and metabolic syndrome in young women after placental syndrome. Obstet Gynecol 2010; 115 (01) 101-108
  • 164 van Rijn BB, Nijdam ME, Bruinse HW. , et al. Cardiovascular disease risk factors in women with a history of early-onset preeclampsia. Obstet Gynecol 2013; 121 (05) 1040-1048
  • 165 Hooijschuur MC, Ghossein-Doha C, Al-Nasiry S, Spaanderman ME. Maternal metabolic syndrome, preeclampsia, and small for gestational age infancy. Am J Obstet Gynecol 2015; 213 (03) 370.e1-370.e7
  • 166 Tobias DK, Chavarro JE, Williams MA. , et al. History of infertility and risk of gestational diabetes mellitus: a prospective analysis of 40,773 pregnancies. Am J Epidemiol 2013; 178 (08) 1219-1225
  • 167 Heitritter SM, Solomon CG, Mitchell GF, Skali-Ounis N, Seely EW. Subclinical inflammation and vascular dysfunction in women with previous gestational diabetes mellitus. J Clin Endocrinol Metab 2005; 90 (07) 3983-3988
  • 168 Retnakaran R, Qi Y, Connelly PW, Sermer M, Zinman B, Hanley AJ. Glucose intolerance in pregnancy and postpartum risk of metabolic syndrome in young women. J Clin Endocrinol Metab 2010; 95 (02) 670-677
  • 169 Retnakaran R, Qi Y, Connelly PW, Sermer M, Hanley AJ, Zinman B. The graded relationship between glucose tolerance status in pregnancy and postpartum levels of low-density-lipoprotein cholesterol and apolipoprotein B in young women: implications for future cardiovascular risk. J Clin Endocrinol Metab 2010; 95 (09) 4345-4353
  • 170 Bellamy L, Casas JP, Hingorani AD, Williams D. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet 2009; 373 (9677): 1773-1779
  • 171 Shah BR, Retnakaran R, Booth GL. Increased risk of cardiovascular disease in young women following gestational diabetes mellitus. Diabetes Care 2008; 31 (08) 1668-1669
  • 172 Carr DB, Utzschneider KM, Hull RL. , et al. Gestational diabetes mellitus increases the risk of cardiovascular disease in women with a family history of type 2 diabetes. Diabetes Care 2006; 29 (09) 2078-2083
  • 173 Fadl H, Magnuson A, Östlund I, Montgomery S, Hanson U, Schwarcz E. Gestational diabetes mellitus and later cardiovascular disease: a Swedish population based case-control study. BJOG 2014; 121 (12) 1530-1536
  • 174 Paneni F, Beckman JA, Creager MA, Cosentino F. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur Heart J 2013; 34 (31) 2436-2443
  • 175 Reichetzeder C, Dwi Putra SE, Pfab T. , et al. Increased global placental DNA methylation levels are associated with gestational diabetes. Clin Epigenetics 2016; 8: 82
  • 176 Maghbooli Z, Larijani B, Emamgholipour S, Amini M, Keshtkar A, Pasalar P. Aberrant DNA methylation patterns in diabetic nephropathy. J Diabetes Metab Disord 2014; 13: 69
  • 177 Zhao J, Goldberg J, Bremner JD, Vaccarino V. Global DNA methylation is associated with insulin resistance: a monozygotic twin study. Diabetes 2012; 61 (02) 542-546
  • 178 Maghbooli Z, Hossein-Nezhad A, Larijani B, Pasalar P, Keshtkar AA. Association between alterations in global DNA methylation and predisposing factors in diabetes: a high pressure liquid chromatography based study. Minerva Med 2015; 106 (04) 221-231
  • 179 Pearce MS, McConnell JC, Potter C. , et al. Global LINE-1 DNA methylation is associated with blood glycaemic and lipid profiles. Int J Epidemiol 2012; 41 (01) 210-217
  • 180 Williams KT, Schalinske KL. Tissue-specific alterations of methyl group metabolism with DNA hypermethylation in the Zucker (type 2) diabetic fatty rat. Diabetes Metab Res Rev 2012; 28 (02) 123-131
  • 181 Zhong J, Xu C, Reece EA, Yang P. The green tea polyphenol EGCG alleviates maternal diabetes-induced neural tube defects by inhibiting DNA hypermethylation. Am J Obstet Gynecol 2016; 215 (03) 368.e1-368.e10