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Placental Vascular Defects in Compromised Pregnancies: Effects of Assisted Reproductive Technologies and Other Maternal Stressors

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Advances in Fetal and Neonatal Physiology

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 814))

Abstract

Many factors negatively affect pregnancy establishment and subsequent fetal growth and development, including maternal factors such as nutritional stress, age, body mass index, and genetic background, and external factors including environmental stress, psychosocial stress, multiple fetuses, medical conditions (e.g., polycystic ovary syndrome), lifestyle choices (e.g., alcohol consumption, smoking), and assisted reproductive technologies. These same factors have similar consequences for placental growth and development, including vascular development. We and others have shown that placental vascular development begins very early in pregnancy and determines, to a large extent, placental function—that is, the magnitude of the increase in placental blood flow and thus nutrient transport to the fetus. During the peri-implantation period and also later in pregnancy, cloned (somatic cell nuclear transfer) embryos exhibit a variety of placental defects including reduced vascularization and altered expression of angiogenic factors. Although placental defects are less pronounced in pregnancies resulting from the transfer of in vitro fertilized embryos, we and others have recently demonstrated that vascularization, expression of angiogenic factors, sex steroid receptors, several epigenetic markers, and growth of utero-placental tissues all were altered during early pregnancy after transfer of embryos obtained through natural mating, in vitro fertilization, or other assisted reproductive techniques. These observations are in agreement with the recent reports that in humans even singleton pregnancies established with assisted reproductive techniques are at increased risk of preterm delivery and low birth weight, and seem especially relevant considering the rapidly expanding use of these techniques in humans and animals.

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References

  1. Reynolds LP, Caton JS, Redmer DA, Grazul-Bilska AT, Vonnahme KA, Borowicz PP, et al. Evidence for altered placental blood flow and vascularity in compromised pregnancies. J Physiol. 2006;572:51–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Reynolds LP, Vonnahme KA, Lemley CO, Redmer DA, Grazul-Bilska AT, Borowicz PP, et al. Maternal stress and placental vascular function and remodeling. Curr Vasc Pharmacol. 2013;11:564–93.

    Article  CAS  PubMed  Google Scholar 

  3. Reynolds LP, Caton JS. Role of the pre- and post-natal environment in developmental programming of health and productivity. Mol Cell Endocrinol. 2012;354:54–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Borowicz PP, Reynolds LP. Placental programming: more may still be less. J Physiol. 2010;588:393.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Martin JA, Hamilton BE, Ventura SJ, Osterman MJ, Kimeyer S, Mathews TJ, et al. Births: final data for 2009. National vital statistics reports, vol 60(1). National Center for Health Statistics, Centers for Disease Control and Prevention, DHHS (online). 2011. (cited 2012). http://www.cdc.gov/nchs/data/nvsr/nvsr60/nvsr60_01.pdf

  6. WHO (World Health Organization). Millenium Development Goal (MDG) 4, Child mortality, Infant mortality rate. Global Health Observatory Database, WHO, 2008. http://apps.who.int/ghodata/

  7. Godfrey KM, Barker DJ. Fetal nutrition and adult disease. Am J Clin Nutr. 2000;71 Suppl 5:1344S–52.

    CAS  PubMed  Google Scholar 

  8. Reynolds LP, Borowicz PP, Caton JS, Vonnahme KA, Luther JS, Buchanan DS, et al. Uteroplacental vascular development and placental function: an update. Int J Dev Biol. 2010;54:355–66.

    Article  CAS  PubMed  Google Scholar 

  9. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8:253–62.

    Article  CAS  PubMed  Google Scholar 

  10. Van den Bergh BR. Developmental programming of early brain and behaviour development and mental health: a conceptual framework. Dev Med Child Neurol. 2011;53 Suppl 4:19–23.

    Article  PubMed  Google Scholar 

  11. Ismail-Beigi F, Catalano PM, Hanson RW. Metabolic programming: fetal origins of obesity and metabolic syndrome in the adult. Am J Physiol Endocrinol Metab. 2006;291:E439–40.

    Article  CAS  PubMed  Google Scholar 

  12. Skinner MK, Manikkam M, Guerrero-Bosagna C. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab. 2010;21:214–22.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Wilmut I, Sales DI, Ashworth CJ. Maternal and embryonic factors associated with prenatal loss in mammals. J Reprod Fertil. 1986;76:851–64.

    Article  CAS  PubMed  Google Scholar 

  14. Reynolds LP, Redmer DA. Mini-review: angiogenesis in the placenta. Biol Reprod. 2001;64:1033–40.

    Article  CAS  PubMed  Google Scholar 

  15. Dixon AB, Knights M, Winkler JL, Marsh DJ, Pate JL, Wilson ME, et al. Patterns of late embryonic and fetal mortality and association with several factors in sheep. J Anim Sci. 2007;85:1274–84.

    Article  CAS  PubMed  Google Scholar 

  16. Teklenburg G, Salker M, Heijnen C, Macklon NS, Brosens JJ. The molecular basis of recurrent pregnancy loss: impaired natural embryo selection. Mol Hum Reprod. 2010;16:886–95.

    Article  CAS  PubMed  Google Scholar 

  17. Reynolds LP, Redmer DA. Utero-placental vascular development and placental function. J Anim Sci. 1995;73:1839–51.

    CAS  PubMed  Google Scholar 

  18. Sinclair KD, Singh R. Modelling the developmental origins of health and disease in the early embryo. Theriogenology. 2007;67:43–53.

    Article  PubMed  Google Scholar 

  19. CDC. National Health and Nutrition Examination Survey (NHANES). Key statistics. Center for Disease Control and Prevention, 2013. http://www.cdc.gov/ncbddd/features/obesity-keyfindings.html

  20. Reynolds LP, Borowicz PP, Caton JS, Vonnahme KA, Luther JS, Hammer CJ, et al. Developmental programming: the concept, large animal models, and the key role of uteroplacental vascular development. J Anim Sci. 2010;88(13 Suppl):E61–72.

    Article  CAS  PubMed  Google Scholar 

  21. Grazul-Bilska AT, Borowicz PP, Johnson ML, Minten MA, Bilski JJ, Wroblewski R, et al. Placental development during early pregnancy in sheep: vascular growth and expression of angiogenic factors in maternal placenta. Reproduction. 2010;140:165–74.

    Article  CAS  PubMed  Google Scholar 

  22. Grazul-Bilska AT, Johnson ML, Borowicz PP, Minten M, Bilski JJ, Wroblewski R, et al. Placental development during early pregnancy in sheep: cell proliferation, global methylation and angiogenesis in fetal placenta. Reproduction. 2011;141:529–40.

    Article  CAS  PubMed  Google Scholar 

  23. Vonnahme KA, Lemley CO, Shukla P, O’Rourke ST. Placental programming: how the maternal environment can impact placental function. J Anim Sci. 2013;91:2467–80.

    Article  CAS  PubMed  Google Scholar 

  24. Meegdes BH, Ingenhoes R, Peeters LL, Exalto N. Early pregnancy wastage: relationship between chorionic vascularization and embryonic development. Fertil Steril. 1988;49:216–20.

    CAS  PubMed  Google Scholar 

  25. Bassil S, Magritte JP, Roth J, Nisolle M, Donnez J, Gordts S. Uterine vascularity during stimulation and its correlation with implantation in in-vitro fertilization. Hum Reprod. 1995;10:1497–501.

    Article  CAS  PubMed  Google Scholar 

  26. Konje JC, Howarth ES, Kaufmann P, Taylor DJ. Longitudinal quantification of uterine artery blood volume flow changes during gestation in pregnancies complicated by intrauterine growth restriction. BJOG. 2003;110:301–5.

    Article  PubMed  Google Scholar 

  27. Mayhew TM, Wijesekara J, Baker PN, Ong SS. Short Communication: morphometric evidence that villous development and fetoplacental angiogenesis are compromised by intrauterine growth restriction but not by pre-eclampsia. Placenta. 2004;25:829–33.

    Article  CAS  PubMed  Google Scholar 

  28. Wulff C, Weigand M, Kreienberg R, Fraser HM. Angiogenesis during primate placentation in health and disease. Reproduction. 2003;126:569–77.

    Article  CAS  PubMed  Google Scholar 

  29. Zygmunt M, Herr F, Munstedt K, Lang U, Liang OD. Angiogenesis and vasculogenesis in pregnancy. Eur J Obstet Gynecol Reprod Biol. 2003;110 Suppl 1:S10–8.

    Article  CAS  PubMed  Google Scholar 

  30. Redmer DA, Aitken RP, Milne JS, Reynolds LP, Wallace JM. Influence of maternal nutrition on messenger RNA expression of placental angiogenic factors and their receptors at midgestation in adolescent sheep. Biol Reprod. 2005;72:1004–9.

    Article  CAS  PubMed  Google Scholar 

  31. Redmer DA, Luther JS, Milne JS, Aitken RP, Johnson ML, Borowicz PP, et al. Fetoplacental growth and vascular development in overnourished adolescent sheep at day 50, 90 and 130 of gestation. Reproduction. 2009;137:749–57.

    Article  CAS  PubMed  Google Scholar 

  32. Tseng JJ, Chou MM. Differential expression of growth-, angiogenesis- and invasion-related factors in the development of placenta accreta. Taiwan J Obstet Gynecol. 2006;45:100–6.

    Article  PubMed  Google Scholar 

  33. Vedmedovska N, Rezeberga D, Teibe U, Melderis I, Donders GG. Placental pathology in fetal growth restriction. Eur J Obstet Gynecol Reprod Biol. 2011;155:36–40.

    Article  PubMed  Google Scholar 

  34. Gourvas V, Dalpa E, Konstantinidou A, Vrachnis N, Spandidos DA, Sifakis S. Angiogenic factors in placentas from pregnancies complicated by fetal growth restriction (review). Mol Med Rep. 2012;6:23–7.

    CAS  PubMed  Google Scholar 

  35. Shimizu T, Hoshino Y, Miyazaki H, Sato E. Angiogenesis and microvasculature in the female reproductive organs: physiological and pathological implications. Curr Pharm Des. 2012;18:303–9.

    Article  CAS  PubMed  Google Scholar 

  36. Anthony RV, Limesand SW, Jeckel KM. Transcriptional regulation in the placenta during normal and compromised fetal growth. Biochem Soc Trans. 2001;29:42048.

    Article  Google Scholar 

  37. Regnault TRH, de Vrijer B, Battaglia FC. Transport and metabolism of amino acids in placenta. Endocrine. 2002;19:23–41.

    Article  CAS  PubMed  Google Scholar 

  38. Belkacemi L, Nelson DM, Desai M, Ross MG. Maternal undernutrition influences placental-fetal development. Biol Reprod. 2010;83:325–31.

    Article  CAS  PubMed  Google Scholar 

  39. Mayhew TM. A stereological perspective on placental morphology in normal and complicated pregnancies. J Anat. 2009;215:77–90.

    Article  PubMed Central  PubMed  Google Scholar 

  40. Zhu MJ, Du M, Nathanielsz PW, Ford SP. Maternal obesity up-regulates inflammatory signaling pathways and enhances cytokine expression in the mid-gestation sheep placenta. Placenta. 2010;31:387–91.

    Article  CAS  PubMed  Google Scholar 

  41. Reynolds LP, Borowicz PP, Vonnahme KA, Johnson ML, Grazul-Bilska AT, Redmer DA, et al. Placental angiogenesis in sheep models of compromised pregnancy. J Physiol. 2005;565:43–58.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Seckl JR. Prenatal glucocorticoids and long-term programming. Eur J Endocrinol. 2004;151 Suppl 3:U49–62.

    Article  CAS  PubMed  Google Scholar 

  43. Seckl JR, Meaney MJ. Glucocorticoid programming. Ann N Y Acad Sci. 2004;1032:63–84.

    Article  CAS  PubMed  Google Scholar 

  44. Gheorghe CP, Goyal R, Mittal A, Longo LD. Gene expression in the placenta: maternal stress and epigenetic responses. Int J Dev Biol. 2010;54:507–23.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Xiong F, Zhang L. Role of the hypothalamic-pituitary-adrenal axis in developmental programming of health and disease. Front Neuroendocrinol. 2013;34:27–46.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Reynolds LP, Grazul-Bilska AT, Redmer DA. Angiogenesis in the female reproductive organs: pathological implications. Int J Exp Pathol. 2002;83:151–63.

    Article  PubMed Central  PubMed  Google Scholar 

  47. Reynolds LP, Redmer DA. Growth and microvascular development of the uterus during early pregnancy in ewes. Biol Reprod. 1992;47:698–708.

    Article  CAS  PubMed  Google Scholar 

  48. Zheng J, Johnson ML, Redmer DA, Reynolds LP. Estrogen and progesterone receptors, cell proliferation, and c-fos expression in the ovine uterus during early pregnancy. Endocrinology. 1996;137:340–8.

    CAS  PubMed  Google Scholar 

  49. Borowicz PP, Arnold DR, Johnson ML, Grazul-Bilska AT, Redmer DA, Reynolds LP. Placental growth throughout the last two-thirds of pregnancy in sheep: vascular development and angiogenic factor expression. Biol Reprod. 2007;76:259–67.

    Article  CAS  PubMed  Google Scholar 

  50. Barnes FL. The effects of the early uterine environment on the subsequent development of embryo and fetus. Theriogenology. 2000;53:649–58.

    Article  CAS  PubMed  Google Scholar 

  51. Cai LY, Izumi S, Koido S, Uchida N, Suzuki T, Matsubayashi H, et al. Abnormal placental cord insertion may induce intrauterine growth restriction in IVF-twin pregnancies. Hum Reprod. 2006;21: 1285–90.

    Article  PubMed  Google Scholar 

  52. Grazul-Bilska AT, Pant D, Luther JS, Borowicz PP, Navanukraw C, Caton JS, et al. Pregnancy rates and gravid uterine parameters in single, twin and triplet pregnancies in naturally bred ewes and ewes after transfer of in vitro produced embryos. Anim Reprod Sci. 2006;92:268–83.

    Article  CAS  PubMed  Google Scholar 

  53. Grazul-Bilska AT, Johnson ML, Borowicz PP, Baranko L, Redmer DA, Reynolds LP. Placental development during early pregnancy in sheep: effects of embryo origin on fetal and placental growth and global methylation. Theriogenology. 2013;79:94–102.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Romundstad LB, Romundstad PR, Sunde A, von Düring V, Skjaerven R, Vatten LJ. Increased risk of placenta previa in pregnancies following IVF/ICSI; a comparison of ART and non-ART pregnancies in the same mother. Hum Reprod. 2006;21:2353–8.

    Article  PubMed  Google Scholar 

  55. Allen C, Bowdin S, Harrison RF, Sutcliffe AG, Brueton L, Kirby G, et al. Pregnancy and perinatal outcomes after assisted reproduction: a comparative study. Ir J Med Sci. 2008;177:233–41.

    Article  CAS  PubMed  Google Scholar 

  56. Collier AC, Miyagi SJ, Yamauchi Y, Ward MA. Assisted reproduction technologies impair placental steroid metabolism. J Steroid Biochem Mol Biol. 2009;116:21–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Delle Piane L, Lin W, Liu X, Donjacour A, Minasi P, Revelli A, et al. Effect of the method of conception and embryo transfer procedure on mid-gestation placenta and fetal development in an IVF mouse model. Hum Reprod. 2010;25:2039–46.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Sellers López F, Orozco-Beltran D, Gil-Guillen V, Lozano JM, Palacios A, Bernabeu R. Analysis of placental vascularization by means of 3D Power Doppler in women pregnant following oocyte donation. Reprod Sci. 2010;17:754–9.

    Article  PubMed  Google Scholar 

  59. Esh-Broder E, Ariel I, Abas-Bashir N, Bdolah Y, Celnikier DH. Placenta accreta is associated with IVF pregnancies: a retrospective chart review. BJOG. 2011;118:1084–9.

    Article  CAS  PubMed  Google Scholar 

  60. Tomic V, Tomic J. Neonatal outcome of IVF singletons versus naturally conceived in women aged 35 years and over. Acta Gynecol Obstet. 2011;284:1411–6.

    Google Scholar 

  61. Holm P, Walker SK, Seamark RF. Embryo viability, duration of gestation and birth weight in sheep after transfer of in vitro matured and in vitro fertilized zygotes cultured in vitro or in vivo. J Reprod Fertil. 1996;107:175–81.

    Article  CAS  PubMed  Google Scholar 

  62. Farin PW, Piedrahita JA, Farin CE. Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology. 2006;65:178–91.

    Article  PubMed  Google Scholar 

  63. Bertolini M, Mason JB, Beam SW, Carneiro GF, Sween ML, Kominek DJ, et al. Morphology and morphometry of in vivo- and in vitro-produced bovine concepti from early pregnancy to term and association with high birth weights. Theriogenology. 2002;58:973–94.

    Article  PubMed  Google Scholar 

  64. Hill JR, Burghardt RC, Jones K, Long CR, Looney CR, Shin T, et al. Evidence for placental abnormality as the major cause of mortality in first-trimester somatic cell cloned bovine fetuses. Biol Reprod. 2000;63:1787–94.

    Article  CAS  PubMed  Google Scholar 

  65. Hill JR, Schlafer DH, Fisher PJ, Davies CJ. Abnormal expression of trophoblast major histocompatibility complex class I antigens in cloned bovine pregnancies is associated with a pronounced endometrial lymphocytic response. Biol Reprod. 2002;67:55–63.

    Article  CAS  PubMed  Google Scholar 

  66. Cetin I, Cozzi V, Antonazzo P. Fetal development after assisted reproduction – a review. Placenta. 2003;24(Suppl B):S104–13.

    Article  PubMed  Google Scholar 

  67. Miles JR, Farin CE, Rodriguez KF, Alexander JE, Farin PW. Angiogenesis and morphometry of bovine placentas in late gestation from embryos produced in vivo or in vitro. Biol Reprod. 2004;71:1919–26.

    Article  CAS  PubMed  Google Scholar 

  68. Miles JR, Farin CE, Rodriguez KF, Alexander JE, Farin PW. Effects of embryo culture on angiogenesis and morphometry of bovine placentas during early gestation. Biol Reprod. 2005;73:663–71.

    Article  CAS  PubMed  Google Scholar 

  69. Arnold DR, Bordignon V, Lefebvre R, Murphy BD, Smith LC. Somatic cell nuclear transfer alters peri-implantation trophoblast differentiation in bovine embryos. Reproduction. 2006;132:279–90.

    Article  CAS  PubMed  Google Scholar 

  70. Miglino MA, Pereira FT, Visintin JA, Garcia JM, Meirelles FV, Rumpf R, et al. Placentation in cloned cattle: structure and microvascular architecture. Theriogenology. 2007;68:604–17.

    Article  CAS  PubMed  Google Scholar 

  71. Palmieri C, Loi P, Reynolds LP, Ptak G, Della Salda L. Placental abnormalities in ovine somatic cell clones at term: a light and electron microscopic investigation. Placenta. 2007;28:577–84.

    Article  CAS  PubMed  Google Scholar 

  72. Palmieri C, Loi P, Ptak G, Della Salda L. Review paper: a review of the pathology of abnormal placentae of somatic cell nuclear transfer clone pregnancies in cattle, sheep, and mice. Vet Pathol. 2008;45: 865–80.

    Article  CAS  PubMed  Google Scholar 

  73. Campos DB, Papa PC, Marques Jr JE, Garbelotti F, Fatima LA, Artoni LP, et al. Somatic cell nuclear transfer is associated with altered expression of angiogenic factor system in bovine placentomes at term. Genet Mol Res. 2010;9:309–23.

    Article  CAS  PubMed  Google Scholar 

  74. Hoffert KA, Batchelder CA, Bertolini M, Moyer AL, Famula TR, Anderson DL, et al. Measures of maternal-fetal interaction in day-30 bovine pregnancies derived from nuclear transfer. Cloning Stem Cells. 2005;7:289–305.

    Article  CAS  PubMed  Google Scholar 

  75. Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, Giraud-Delville C, et al. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci U S A. 2009;106:5687–92.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. Fleming TP, Kwong WY, Porter R, Ursell E, Fesenko I, Wilkins A, et al. The embryo and its future. Biol Reprod. 2004;71:1046–54.

    Article  CAS  PubMed  Google Scholar 

  77. Coan PM, Vaughan OR, Sekita Y, Finn SL, Burton GJ, Constancia M, et al. Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J Physiol. 2010;588:527–38.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Iliadou AN, Janson PC, Cnattingius S. Epigenetics and assisted reproductive technology. J Intern Med. 2011;270:414–20.

    Article  CAS  PubMed  Google Scholar 

  79. Watt AM, Elshaug AG, Willis CD, Hiller JE. ASTUTE Health study group. Assisted reproductive technologies: a systematic review of safety and effectiveness to inform disinvestment policy. Health Policy. 2011;102:200–13.

    Article  PubMed  Google Scholar 

  80. Ceelen M, van Weissenbruch MM, Vermeiden JPW, van Leeuwen FE, Delemarre-van de Waal HA. Growth and development of children born after in vitro fertilization. Fertil Steril. 2008;90:1662–73.

    Article  PubMed  Google Scholar 

  81. Ptak GE, D’Agostino A, Toschi P, Fidanza A, Zacchini F, Czernik M, et al. Post-implantation mortality of in vitro produced embryos is associated with DNA methyltransferase 1 dysfunction in sheep placenta. Hum Reprod. 2013;28:298–305.

    Article  CAS  PubMed  Google Scholar 

  82. Bourc’his D, Le Bourhis D, Patin D, Niveleau A, Comizzoli P, Renard JP, et al. Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos. Curr Biol. 2001;11: 1542–6.

    Article  PubMed  Google Scholar 

  83. Beaujean N, Taylor J, Gardner J, Wilmut I, Meehan R, Young L. Effect of limited DNA methylation reprogramming in the normal sheep embryo on somatic cell nuclear transfer. Biol Reprod. 2004;71:185–93.

    Article  CAS  PubMed  Google Scholar 

  84. Suteevun T, Parnpai R, Smith SL, Chang CC, Muenthaisong S, Tian XC. Epigenetic characteristics of cloned and in vitro-fertilized swamp buffalo (Bubalus bubalis) embryos. J Anim Sci. 2006;84: 2065–71.

    Article  CAS  PubMed  Google Scholar 

  85. de Waal E, Yamazaki Y, Ingale P, Bartolemei M, Yanagimachi R, McCarrey JR. Gonadotropin stimulation contributes to an increased incidence of epimutations in ICSI-derived mice. Hum Mol Genet. 2012; 21:4460–72.

    Article  PubMed Central  PubMed  Google Scholar 

  86. de Waal E, Yamazaki Y, Ingale P, Bartolemei M, Yanagimachi R, McCarrey JR. Primary epimutations introduced during intracytoplasmic sperm injection (ICSI) are corrected by germline-specific epigenetic reprogramming. Proc Natl Acad Sci U S A. 2012;109:4163–8.

    Article  PubMed Central  PubMed  Google Scholar 

  87. Bressan FF, De Bem TH, Perecin F, Lopes FL, Ambrosio CE, Meirelles FV, et al. Unearthing the roles of imprinted genes in the placenta. Placenta. 2009;30:823–34.

    Article  CAS  PubMed  Google Scholar 

  88. Mesquita FS, Machado SA, Drnevich J, Borowicz P, Wang Z, Nowak RA. Influence of cloning by chromatin transfer on placental gene expression at Day 45 of pregnancy in cattle. Anim Reprod Sci. 2013;136:231–44.

    Article  CAS  PubMed  Google Scholar 

  89. Caton JS, Hess BW. Maternal plane of nutrition: impacts on fetal outcomes and postnatal offspring responses. In: Hess BW, DelCurto T, Bowman JG, Waterman RC, editors. Proceedings of 4th grazing livestock nutrition conference. Champaign, IL: West Sect Am Soc Anim Sci; 2010. p. 104–22. http://coronasc.nmsu.edu/documents/proceedings_of_the_fourth_glnc_2010.pdf#page=112.

    Google Scholar 

  90. Funston RN, Larson DM, Vonnahme KA. Effects of maternal nutrition on conceptus growth and offspring performance: implications for beef cattle production. J Anim Sci. 2010;88 Suppl 13:E205–15.

    Article  CAS  PubMed  Google Scholar 

  91. Funston RN, Summers AF, Roberts AJ. Alpharma beef cattle nutrition symposium: implications of nutritional management for beef cow-calf systems. J Anim Sci. 2012;90:2301–7.

    Article  CAS  PubMed  Google Scholar 

  92. McKnight JR, Satterfield MC, Li X, Gao H, Wang J, Li D, et al. Obesity in pregnancy: problems and potential solutions. Front Biosci (Elite Ed). 2011;3: 442–52.

    Article  Google Scholar 

  93. Wang J, Wu Z, Li D, Li N, Dindot SV, Satterfield MC, et al. Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal. 2012;17:282–301.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  94. DelCurto H, Wu G, Satterfield MC. Nutrition and reproduction: links to epigenetics and metabolic syndrome in offspring. Curr Opin Clin Nutr Metab Care. 2013;16:385–91.

    Article  CAS  PubMed  Google Scholar 

  95. Wu G, Bazer FW, Satterfield MC, Li X, Wang X, Johnson GA, et al. Impacts of arginine nutrition on embryonic and fetal development in mammals. Amino Acids. 2013;45:241–56.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Center for Nutrition and Pregnancy, North Dakota State University, Fargo, ND, USA

    Lawrence P. Reynolds, Pawel P. Borowicz & Anna T. Grazul-Bilska

  2. Department of Animal Sciences, North Dakota State University, Fargo, ND, 58108-6050, USA

    Lawrence P. Reynolds, Pawel P. Borowicz & Anna T. Grazul-Bilska

  3. School of Veterinary Science, The University of Queensland, Gatton, QLD, 4343, Australia

    Chiara Palmieri

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  1. Lawrence P. Reynolds
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  2. Pawel P. Borowicz
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  3. Chiara Palmieri
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  4. Anna T. Grazul-Bilska
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Correspondence to Lawrence P. Reynolds .

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Editors and Affiliations

  1. Center for Perinatal Biology, Loma Linda University School of Medicine, Loma Linda, California, USA

    Lubo Zhang

  2. Center for Perinatal Biology, Loma Linda University School of Medicine, Loma Linda, California, USA

    Charles A. Ducsay

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Reynolds, L.P., Borowicz, P.P., Palmieri, C., Grazul-Bilska, A.T. (2014). Placental Vascular Defects in Compromised Pregnancies: Effects of Assisted Reproductive Technologies and Other Maternal Stressors. In: Zhang, L., Ducsay, C. (eds) Advances in Fetal and Neonatal Physiology. Advances in Experimental Medicine and Biology, vol 814. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1031-1_17

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