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PMID: 25699984 Published · epublish English Journal Article Research Support, Non-U.S. Gov't Review

The periconceptional environment and cardiovascular disease: does in vitro embryo culture and transfer influence cardiovascular development and health?

Nutrients ·Vol. 7 ·No. 3 ·2015-02-18 ·Pages 1378-425

Padhee M, Zhang S, Lie S, Wang KC, Botting KJ, McMillen IC, MacLaughlin SM, Morrison JL

Abstract

Assisted Reproductive Technologies (ARTs) have revolutionised reproductive medicine; however, reports assessing the effects of ARTs have raised concerns about the immediate and long-term health outcomes of the children conceived through ARTs. ARTs include manipulations during the periconceptional period, which coincides with an environmentally sensitive period of gamete/embryo development and as such may alter cardiovascular development and health of the offspring in postnatal life. In order to identify the association between ARTs and cardiovascular health outcomes, it is important to understand the events that occur during the periconceptional period and how they are affected by procedures involved in ARTs. This review will highlight the emerging evidence implicating adverse cardiovascular outcomes before and after birth in offspring conceived through ARTs in both human and animal studies. In addition, it will identify the potential underlying causes and molecular mechanisms responsible for the congenital and adult cardiovascular dysfunctions in offspring whom were conceived through ARTs.

MeSH Terms
Animals Cardiovascular Diseases/etiology Embryonic Development Female Fertilization in Vitro/adverse effects Humans Pregnancy Pregnancy Outcome
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Padhee Monalisa
Early Origins of Adult Health Research Group, School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA 5001, Australia. [email protected].
Zhang Song
Early Origins of Adult Health Research Group, School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA 5001, Australia. [email protected].
Lie Shervi
Early Origins of Adult Health Research Group, School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA 5001, Australia. [email protected].
Wang Kimberley C
Early Origins of Adult Health Research Group, School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA 5001, Australia. [email protected].
Botting Kimberley J
Early Origins of Adult Health Research Group, School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA 5001, Australia. [email protected].
McMillen I Caroline
Early Origins of Adult Health Research Group, School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA 5001, Australia. [email protected].
MacLaughlin Severence M
Early Origins of Adult Health Research Group, School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA 5001, Australia. [email protected].
Morrison Janna L
Early Origins of Adult Health Research Group, School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA 5001, Australia. [email protected].
References (255)
255 references, click to expand
  1. Epigenetics and cardiovascular development.
    Annu Rev Physiol. 2012;74:41-68 PMID: 22035349
  2. Imprinted gene expression in fetal growth and development.
    Placenta. 2012 Jun;33(6):480-6 PMID: 22465419
  3. Epigenetic reprogramming in mammals.
    Hum Mol Genet. 2005 Apr 15;14 Spec No 1:R47-58 PMID: 15809273
  4. Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring.
    PLoS One. 2010;5(12):e15558 PMID: 21179452
  5. Maternal periconceptional alcohol consumption and risk for conotruncal heart defects.
    Birth Defects Res A Clin Mol Teratol. 2003 Oct;67(10):875-8 PMID: 14745941
  6. Study of non-muscle cells of the adult mammalian heart: a fine structural analysis and distribution.
    Cytobios. 1980;28(109):41-61 PMID: 7428441
  7. Sizing up the heart: development redux in disease.
    Genes Dev. 2003 Aug 15;17(16):1937-56 PMID: 12893779
  8. Culture and selection of viable blastocysts: a feasible proposition for human IVF?
    Hum Reprod Update. 1997 Jul-Aug;3(4):367-82 PMID: 9459282
  9. Selective single blastocyst transfer reduces the multiple pregnancy rate and increases pregnancy rates: a pre- and postintervention study.
    BJOG. 2008 Feb;115(3):385-90 PMID: 18190376
  10. Hox genes and the evolution of vertebrate axial morphology.
    Development. 1995 Feb;121(2):333-46 PMID: 7768176
  11. Epigenetics and the environment.
    Ann N Y Acad Sci. 2003 Mar;983:151-60 PMID: 12724220
  12. Epigenetic risks related to assisted reproductive technologies: risk analysis and epigenetic inheritance.
    Hum Reprod. 2002 Oct;17(10):2487-94 PMID: 12351517
  13. Aberrant fetal growth and development after in vitro culture of sheep zygotes.
    J Reprod Fertil. 1999 May;116(1):177-86 PMID: 10505068
  14. Culture of viable human blastocysts in defined sequential serum-free media.
    Hum Reprod. 1998 Jun;13 Suppl 3:148-59; discussion 160 PMID: 9755421
  15. The epigenetic imprinting defect of patients with Beckwith-Wiedemann syndrome born after assisted reproductive technology is not restricted to the 11p15 region.
    J Med Genet. 2006 Dec;43(12):902-7 PMID: 16825435
  16. Regulation of zygotic gene activation in the mouse.
    Bioessays. 1993 Aug;15(8):531-8 PMID: 8135766
  17. Clinical and molecular genetic features of Beckwith-Wiedemann syndrome associated with assisted reproductive technologies.
    Hum Reprod. 2009 Mar;24(3):741-7 PMID: 19073614
  18. Cardiomyocyte proliferation contributes to heart growth in young humans.
    Proc Natl Acad Sci U S A. 2013 Jan 22;110(4):1446-51 PMID: 23302686
  19. Blastocyst environment and its influence on offspring cardiovascular health: the heart of the matter.
    J Anat. 2009 Jul;215(1):52-9 PMID: 19215321
  20. Mismatched pre- and postnatal nutrition leads to cardiovascular dysfunction and altered renal function in adulthood.
    Proc Natl Acad Sci U S A. 2007 May 29;104(22):9529-33 PMID: 17483483
  21. The molecular foundations of the maternal to zygotic transition in the preimplantation embryo.
    Hum Reprod Update. 2002 Jul-Aug;8(4):323-31 PMID: 12206467
  22. Regulation of ovarian follicular development in primates: facts and hypotheses.
    Endocr Rev. 1996 Apr;17(2):121-55 PMID: 8706629
  23. IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch.
    Mol Hum Reprod. 2005 Sep;11(9):631-40 PMID: 16219628
  24. Common carotid intima-media thickness and arterial stiffness: indicators of cardiovascular risk in high-risk patients. The SMART Study (Second Manifestations of ARTerial disease).
    Circulation. 1999 Aug 31;100(9):951-7 PMID: 10468526
  25. Maternal obesity and the early origins of childhood obesity: weighing up the benefits and costs of maternal weight loss in the periconceptional period for the offspring.
    Exp Diabetes Res. 2011;2011:585749 PMID: 22203829
  26. Long-term effect of in vitro culture of mouse embryos with serum on mRNA expression of imprinting genes, development, and behavior.
    Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):5880-5 PMID: 15079084
  27. Implications of epigenetics and genomic imprinting in assisted reproductive technologies.
    Mol Reprod Dev. 2009 Nov;76(11):1006-18 PMID: 19484754
  28. Suboptimal in vitro culture conditions: an epigenetic origin of long-term health effects.
    Mol Reprod Dev. 2007 Sep;74(9):1149-56 PMID: 17474101
  29. Blood pressure response to psychological stressors in adults after prenatal exposure to the Dutch famine.
    J Hypertens. 2006 Sep;24(9):1771-8 PMID: 16915026
  30. Ovarian stimulation and endometrial receptivity.
    Hum Reprod. 1999 Dec;14 Suppl 2:107-11 PMID: 10690806
  31. Improved pregnancy rate in human in vitro fertilization with the use of a medium based on the composition of human tubal fluid.
    Fertil Steril. 1985 Oct;44(4):493-8 PMID: 3902512
  32. Superovulation of female mice delays embryonic and fetal development.
    Hum Reprod. 2001 Jun;16(6):1237-43 PMID: 11387298
  33. Epigenetic mechanisms in cardiac development and disease.
    Acta Biochim Biophys Sin (Shanghai). 2012 Jan;44(1):92-102 PMID: 22194017
  34. Economical and ecological importance of indigenous livestock and the application of assisted reroduction to their preservation.
    Theriogenology. 2000 Jan 1;53(1):149-62 PMID: 10735070
  35. Children born after assisted fertilization have an increased rate of major congenital anomalies.
    Fertil Steril. 2005 Nov;84(5):1300-7 PMID: 16275218
  36. The developmental origins of adult disease (Barker) hypothesis.
    Aust N Z J Obstet Gynaecol. 2006 Feb;46(1):4-14 PMID: 16441686
  37. Effect of periconceptional undernutrition and gender on hypothalamic-pituitary-adrenal axis function in young adult sheep.
    J Endocrinol. 2006 Aug;190(2):203-12 PMID: 16899555
  38. Systemic and pulmonary vascular dysfunction in children conceived by assisted reproductive technologies.
    Circulation. 2012 Apr 17;125(15):1890-6 PMID: 22434595
  39. Transfer of a human zygote.
    Lancet. 1973 Sep 29;2(7831):728-9 PMID: 4125805
  40. Major advances associated with reproduction in dairy cattle.
    J Dairy Sci. 2006 Apr;89(4):1254-66 PMID: 16537958
  41. Gene expression during oogenesis and oocyte development in mammals.
    Dev Biol (N Y 1985). 1985;1:453-524 PMID: 2481471
  42. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice.
    FASEB J. 1998 Aug;12(11):949-57 PMID: 9707167
  43. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific.
    Hum Mol Genet. 2009 Nov 1;18(21):4046-53 PMID: 19656776
  44. In-utero overgrowth in ruminants following embryo culture: lessons from mice and a warning to men.
    Hum Reprod. 2000 Dec;15 Suppl 5:68-86 PMID: 11263539
  45. DNA methylation and gene expression differences in children conceived in vitro or in vivo.
    Hum Mol Genet. 2009 Oct 15;18(20):3769-78 PMID: 19605411
  46. An imprinted gene network that controls mammalian somatic growth is down-regulated during postnatal growth deceleration in multiple organs.
    Am J Physiol Regul Integr Comp Physiol. 2008 Jul;295(1):R189-96 PMID: 18448610
  47. Periconceptional nutrition programs development of the cardiovascular system in the fetal sheep.
    Am J Physiol Regul Integr Comp Physiol. 2002 Sep;283(3):R669-79 PMID: 12185002
  48. Fetal growth restriction and the programming of heart growth and cardiac insulin-like growth factor 2 expression in the lamb.
    J Physiol. 2011 Oct 1;589(Pt 19):4709-22 PMID: 21807611
  49. Endothelial dysfunction: a marker of atherosclerotic risk.
    Arterioscler Thromb Vasc Biol. 2003 Feb 1;23(2):168-75 PMID: 12588755
  50. Neonatal outcome and congenital malformations in children born after in-vitro fertilization.
    Hum Reprod. 2002 May;17(5):1391-8 PMID: 11980770
  51. Ontogeny of expression of a receptor for platelet-activating factor in mouse preimplantation embryos and the effects of fertilization and culture in vitro on its expression.
    Biol Reprod. 1999 Mar;60(3):674-82 PMID: 10026115
  52. Growth during infancy and early childhood in relation to blood pressure and body fat measures at age 8-18 years of IVF children and spontaneously conceived controls born to subfertile parents.
    Hum Reprod. 2009 Nov;24(11):2788-95 PMID: 19648588
  53. A review of known imprinting syndromes and their association with assisted reproduction technologies.
    Hum Reprod. 2008 Dec;23(12):2826-34 PMID: 18703582
  54. Cytokine cross-talk between mother and the embryo/placenta.
    J Reprod Immunol. 2001 Oct-Nov;52(1-2):15-33 PMID: 11600175
  55. Development of follicles in the mammalian ovary.
    Int Rev Cytol. 1991;124:43-101 PMID: 2001918
  56. Genomic imprinting: parental influence on the genome.
    Nat Rev Genet. 2001 Jan;2(1):21-32 PMID: 11253064
  57. Epigenetics and the germline.
    Reproduction. 2005 Feb;129(2):137-49 PMID: 15695608
  58. ESHRE guidelines for good practice in IVF laboratories. Committee of the Special Interest Group on Embryology of the European Society of Human Reproduction and Embryology.
    Hum Reprod. 2000 Oct;15(10):2241-6 PMID: 11006207
  59. Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring.
    J Physiol. 2008 Apr 15;586(8):2231-44 PMID: 18308825
  60. Activation of embryonic genes during preimplantation rat development.
    Mol Reprod Dev. 1994 May;38(1):30-5 PMID: 8049062
  61. Periconceptional undernutrition in sheep accelerates maturation of the fetal hypothalamic-pituitary-adrenal axis in late gestation.
    Endocrinology. 2004 Sep;145(9):4278-85 PMID: 15205376
  62. The longer-term health outcomes for children born as a result of IVF treatment. Part II--Mental health and development outcomes.
    Hum Reprod Update. 2013 May-Jun;19(3):244-50 PMID: 23449643
  63. Congenital malformations in infants born after in vitro fertilization in Sweden.
    Birth Defects Res A Clin Mol Teratol. 2010 Mar;88(3):137-43 PMID: 20063307
  64. Periconception maternal characteristics and embryonic growth trajectories: the Rotterdam Predict study.
    Hum Reprod. 2013 Dec;28(12):3188-96 PMID: 24105824
  65. Genomic imprinting and assisted reproduction.
    Reprod Health. 2004 Oct 26;1(1):6 PMID: 15507137
  66. Uterine histotroph and conceptus development: select nutrients and secreted phosphoprotein 1 affect mechanistic target of rapamycin cell signaling in ewes.
    Biol Reprod. 2011 Dec;85(6):1094-107 PMID: 21865556
  67. Primary prevention of coronary heart disease in women through diet and lifestyle.
    N Engl J Med. 2000 Jul 6;343(1):16-22 PMID: 10882764
  68. In vitro maturation of human oocytes for assisted reproduction.
    Fertil Steril. 2006 Nov;86(5):1277-91 PMID: 16996508
  69. Effect of male age on fertility: evidence for the decline in male fertility with increasing age.
    Fertil Steril. 2003 Jun;79 Suppl 3:1520-7 PMID: 12801554
  70. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes.
    Biol Reprod. 2001 Mar;64(3):918-26 PMID: 11207209
  71. Assisted reproductive technologies are associated with cardiovascular remodeling in utero that persists postnatally.
    Circulation. 2013 Sep 24;128(13):1442-50 PMID: 23985787
  72. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture.
    Nat Genet. 2001 Feb;27(2):153-4 PMID: 11175780
  73. Assisted reproductive technology, epigenetics, and long-term health: a developmental time bomb still ticking.
    Semin Reprod Med. 2009 Sep;27(5):409-16 PMID: 19711251
  74. Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny.
    J Physiol. 2006 Apr 1;572(Pt 1):97-108 PMID: 16497715
  75. Review of media used in ART laboratories.
    J Androl. 2000 Sep-Oct;21(5):610-5 PMID: 10975406
  76. Periconceptional undernutrition alters growth trajectory and metabolic and endocrine responses to fasting in late-gestation fetal sheep.
    Pediatr Res. 2005 Apr;57(4):591-8 PMID: 15695605
  77. Effects of different reproduction techniques: AI MOET or IVP, on health and welfare of bovine offspring.
    Theriogenology. 2000 Jan 15;53(2):575-97 PMID: 10735051
  78. Maternal smoking and congenital heart defects.
    Pediatrics. 2008 Apr;121(4):e810-6 PMID: 18381510
  79. Coronary heart disease after prenatal exposure to the Dutch famine, 1944-45.
    Heart. 2000 Dec;84(6):595-8 PMID: 11083734
  80. Relation of weight and rate of increase in weight during childhood and adolescence to body size, blood pressure, fasting insulin, and lipids in young adults. The Minneapolis Children's Blood Pressure Study.
    Circulation. 1999 Mar 23;99(11):1471-6 PMID: 10086972
  81. Epigenetic reprogramming in mammalian development.
    Science. 2001 Aug 10;293(5532):1089-93 PMID: 11498579
  82. Periconceptional undernutrition in sheep affects adult phenotype only in males.
    J Nutr Metab. 2012;2012:123610 PMID: 23091706
  83. Early onset of coronary artery disease after prenatal exposure to the Dutch famine.
    Am J Clin Nutr. 2006 Aug;84(2):322-7; quiz 466-7 PMID: 16895878
  84. Blastocysts don't go it alone. Extrinsic signals fine-tune the intrinsic developmental program of trophoblast cells.
    Dev Biol. 2005 Apr 15;280(2):260-80 PMID: 15882572
  85. Congenital anomalies in infants conceived by assisted reproductive techniques.
    Arch Iran Med. 2012 Apr;15(4):228-31 PMID: 22424041
  86. Altered pregnancy outcomes in mice following treatment with the hyperglycaemia mimetic, glucosamine, during the periconception period.
    Reprod Fertil Dev. 2013;25(2):405-16 PMID: 23445817
  87. Fetal, infant, and childhood growth and adult blood pressure: a longitudinal study from birth to 22 years of age.
    Circulation. 2002 Mar 5;105(9):1088-92 PMID: 11877360
  88. Embryonic origins of health: long-term effects of IVF in human and livestock.
    Theriogenology. 2000 Jan 15;53(2):537-47 PMID: 10735048
  89. Gamete intra-fallopian transfer.
    Med J Aust. 1985 Oct 28;143(9):428 PMID: 4058357
  90. Pregnancy in aged rats that were born small: cardiorenal and metabolic adaptations and second-generation fetal growth.
    FASEB J. 2012 Oct;26(10):4337-47 PMID: 22772163
  91. Cell allocation to the inner cell mass and the trophectoderm in bovine embryos cultured in two different media.
    Mol Reprod Dev. 1996 Oct;45(2):171-82 PMID: 8914075
  92. Assisted reproductive technology: the state of the ART.
    Ann Med. 1997 Jun;29(3):207-14 PMID: 9240626
  93. Clinical practice. In vitro fertilization.
    N Engl J Med. 2007 Jan 25;356(4):379-86 PMID: 17251534
  94. Risk of congenital heart defects associated with assisted reproductive technologies: a population-based evaluation.
    Eur Heart J. 2011 Feb;32(4):500-8 PMID: 21138932
  95. Role for DNA methylation in genomic imprinting.
    Nature. 1993 Nov 25;366(6453):362-5 PMID: 8247133
  96. Gamete intrafallopian transfer (GIFT): historic perspective.
    J In Vitro Fert Embryo Transf. 1991 Feb;8(1):1-4 PMID: 2016559
  97. Errors in development of fetuses and placentas from in vitro-produced bovine embryos.
    Theriogenology. 2006 Jan 7;65(1):178-91 PMID: 16266745
  98. Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span.
    J Clin Invest. 2013 Dec;123(12):5052-60 PMID: 24270419
  99. Programming of adult cardiovascular function after early maternal undernutrition in sheep.
    Am J Physiol Regul Integr Comp Physiol. 2004 Jul;287(1):R12-20 PMID: 14975924
  100. Epigenetic reprogramming during early development in mammals.
    Reproduction. 2004 Jun;127(6):643-51 PMID: 15175501
  101. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition.
    Basic Clin Pharmacol Toxicol. 2008 Feb;102(2):82-9 PMID: 18226059
  102. Early origins of heart disease: low birth weight and the role of the insulin-like growth factor system in cardiac hypertrophy.
    Clin Exp Pharmacol Physiol. 2012 Nov;39(11):958-64 PMID: 22774980
  103. The timing of the "fertile window" in the menstrual cycle: day specific estimates from a prospective study.
    BMJ. 2000 Nov 18;321(7271):1259-62 PMID: 11082086
  104. The impact of ovarian stimulation on implantation and fetal development in mice.
    Hum Reprod. 2001 Feb;16(2):221-5 PMID: 11157810
  105. Myocyte enlargement, differentiation, and proliferation kinetics in the fetal sheep heart.
    J Appl Physiol (1985). 2007 Mar;102(3):1130-42 PMID: 17122375
  106. Optimization and simplification of culture conditions in human in vitro fertilization (IVF) and preembryo replacement by serum-free media.
    J In Vitro Fert Embryo Transf. 1990 Feb;7(1):47-53 PMID: 2338516
  107. Epigenetics and cardiovascular disease.
    Nat Rev Cardiol. 2010 Sep;7(9):510-9 PMID: 20603647
  108. In vitro fertilization is associated with an increase in major birth defects.
    Fertil Steril. 2005 Nov;84(5):1308-15 PMID: 16275219
  109. Superovulation in mice alters the methylation pattern of imprinted genes in the sperm of the offspring.
    Reprod Toxicol. 2009 Dec;28(4):536-41 PMID: 19549566
  110. Side of ovulation and cycle characteristics in normally fertile women.
    Hum Reprod. 2000 Apr;15(4):752-5 PMID: 10739814
  111. Mitoses and binucleated cells in perinatal human hearts.
    Virchows Arch B Cell Pathol Incl Mol Pathol. 1985;48(1):59-67 PMID: 2858939
  112. Developmental consequences of embryo and cell manipulation in mice and farm animals.
    Reproduction. 2001 Oct;122(4):507-18 PMID: 11570957
  113. Selective loss of imprinting in the placenta following preimplantation development in culture.
    Development. 2004 Aug;131(15):3727-35 PMID: 15240554
  114. In vitro fertilization/embryo transfer in unexplained infertility and minimal peritoneal endometriosis.
    Acta Obstet Gynecol Scand. 1995 Aug;74(7):539-43 PMID: 7618453
  115. Transfer of bovine embryos produced in vivo or in vitro: survival and fetal development.
    Biol Reprod. 1995 Mar;52(3):676-82 PMID: 7756461
  116. Reproduction in females: the role of the early life environment.
    Hum Reprod Update. 2011 Mar-Apr;17(2):210-27 PMID: 20961922
  117. Gamete intra-fallopian transfer (GIFT): a new treatment for infertility.
    Int J Fertil. 1985;30(1):41-5 PMID: 2862118
  118. Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age.
    PLoS One. 2011;6(12):e28745 PMID: 22194901
  119. Cleavage anomalies in early human embryos and survival after prolonged culture in-vitro.
    Hum Reprod. 2000 Dec;15(12):2634-43 PMID: 11098037
  120. In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene.
    Am J Hum Genet. 2003 May;72(5):1338-41 PMID: 12772698
  121. The risk for four specific congenital heart defects associated with assisted reproductive techniques: a population-based evaluation.
    Hum Reprod. 2013 Feb;28(2):367-74 PMID: 23178272
  122. Embryo culture media and IVF/ICSI success rates: a systematic review.
    Hum Reprod Update. 2013 May-Jun;19(3):210-20 PMID: 23385469
  123. Reflections on the golden anniversary of the first embryo transfer to produce a calf.
    Theriogenology. 2000 Jan 1;53(1):3-10 PMID: 10735057
  124. IVF/ICSI twin pregnancies: risks and prevention.
    Hum Reprod Update. 2005 Nov-Dec;11(6):575-93 PMID: 16123055
  125. Zygote intrafallopian transfer (ZIFT): evaluation of 42 cases.
    Fertil Steril. 1988 Sep;50(3):519-21 PMID: 3410103
  126. Plasma pigment epithelium-derived factor is positively associated with obesity in Caucasian subjects, in particular with the visceral fat depot.
    Eur J Endocrinol. 2008 Dec;159(6):713-8 PMID: 18787046
  127. Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function.
    J Physiol. 2012 May 1;590(Pt 9):2167-80 PMID: 22411006
  128. Mammalian embryo culture in the absence of serum or somatic cell support.
    Cell Biol Int. 1994 Dec;18(12):1163-79 PMID: 7703956
  129. In vitro fertilization (IVF) in Sweden: risk for congenital malformations after different IVF methods.
    Birth Defects Res A Clin Mol Teratol. 2005 Mar;73(3):162-9 PMID: 15678490
  130. Zygote intrafallopian transfer as a successful treatment for unexplained infertility.
    Fertil Steril. 1989 Aug;52(2):246-9 PMID: 2666176
  131. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development.
    J Mol Cell Cardiol. 1996 Aug;28(8):1737-46 PMID: 8877783
  132. Ovine fetal development is more sensitive to perturbation by the presence of serum in embryo culture before rather than after compaction.
    Theriogenology. 2007 Feb;67(3):639-47 PMID: 17070902
  133. Imprinted gene expression in the rat embryo-fetal axis is altered in response to periconceptional maternal low protein diet.
    Reproduction. 2006 Aug;132(2):265-77 PMID: 16885535
  134. Cardiomyocyte DNA synthesis and binucleation during murine development.
    Am J Physiol. 1996 Nov;271(5 Pt 2):H2183-9 PMID: 8945939
  135. Effects of pre- and periconceptional undernutrition on arterial function in adult female sheep are vascular bed dependent.
    Exp Physiol. 2009 Sep;94(9):1024-33 PMID: 19561141
  136. Methylation analysis of KvDMR1 in human oocytes.
    J Med Genet. 2007 Feb;44(2):144-7 PMID: 16950814
  137. Congenital malformations in 4224 children conceived after IVF.
    Hum Reprod. 2002 Aug;17(8):2089-95 PMID: 12151442
  138. Assisted reproductive technologies in the reproductive management of small ruminants.
    Anim Reprod Sci. 2012 Feb;130(3-4):152-61 PMID: 22381207
  139. Epigenetics and assisted reproductive technology: a call for investigation.
    Am J Hum Genet. 2004 Apr;74(4):599-609 PMID: 14991528
  140. Cardiomyocyte cell cycle control and growth estimation in vivo--an analysis based on cardiomyocyte nuclei.
    Cardiovasc Res. 2010 Jun 1;86(3):365-73 PMID: 20071355
  141. Imprinted genes and their role in human fetal growth.
    Cytogenet Genome Res. 2006;113(1-4):262-70 PMID: 16575189
  142. Congenital malformations after in-vitro fertilisation.
    Lancet. 1987 Dec 12;2(8572):1392-3 PMID: 2890969
  143. Long-term effects on offspring of exposure of oocytes and embryos to chemical and physical agents.
    Hum Reprod Update. 2000 Nov-Dec;6(6):564-77 PMID: 11129689
  144. Beckwith-Wiedemann syndrome and IVF: a case-control study.
    Am J Hum Genet. 2004 Sep;75(3):526-8 PMID: 15284956
  145. In vitro fertilization and embryo culture strongly impact the placental transcriptome in the mouse model.
    PLoS One. 2010;5(2):e9218 PMID: 20169163
  146. Periconception window: advising the pregnancy-planning couple.
    Fertil Steril. 2008 Feb;89(2 Suppl):e119-21 PMID: 18308052
  147. Delaying childbearing: effect of age on fecundity and outcome of pregnancy.
    BMJ. 1991 Jun 8;302(6789):1361-5 PMID: 2059713
  148. The maternal to zygotic transition in mammals.
    Mol Aspects Med. 2013 Oct;34(5):919-38 PMID: 23352575
  149. Transmission of raised blood pressure and endothelial dysfunction to the F2 generation induced by maternal protein restriction in the F0, in the absence of dietary challenge in the F1 generation.
    Br J Nutr. 2008 Oct;100(4):760-6 PMID: 18304387
  150. Assisted reproduction: the epigenetic perspective.
    Hum Reprod Update. 2005 Sep-Oct;11(5):473-82 PMID: 15994847
  151. Impact of elective single embryo transfer on the twin pregnancy rate.
    Hum Reprod. 2003 Jul;18(7):1449-53 PMID: 12832371
  152. The developmental origins of adult disease.
    Eur J Epidemiol. 2003;18(8):733-6 PMID: 12974544
  153. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension.
    Development. 2000 Oct;127(19):4195-202 PMID: 10976051
  154. Assessment of human oocyte developmental competence by cumulus cell morphology and circulating hormone profile.
    Reprod Biomed Online. 2007 Jan;14(1):49-56 PMID: 17207331
  155. Impact of the periconceptional environment on the programming of adult disease.
    J Dev Orig Health Dis. 2010 Apr;1(2):87-95 PMID: 25143062
  156. Ovarian follicular growth and development in mammals.
    Biol Reprod. 1994 Feb;50(2):225-32 PMID: 8142540
  157. Association between arterial stiffness and atherosclerosis: the Rotterdam Study.
    Stroke. 2001 Feb;32(2):454-60 PMID: 11157182
  158. Embryo culture medium: which is the best?
    Best Pract Res Clin Obstet Gynaecol. 2007 Feb;21(1):83-100 PMID: 17090393
  159. Timing of compaction and inner cell allocation in bovine embryos produced in vivo after superovulation.
    Biol Reprod. 1997 Nov;57(5):1041-9 PMID: 9369168
  160. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo.
    Biol Reprod. 2000 Jun;62(6):1526-35 PMID: 10819752
  161. The embryo and its future.
    Biol Reprod. 2004 Oct;71(4):1046-54 PMID: 15215194
  162. Regulation of supply and demand for maternal nutrients in mammals by imprinted genes.
    J Physiol. 2003 Feb 15;547(Pt 1):35-44 PMID: 12562908
  163. Absence of insulin resistance and low-grade inflammation despite early metabolic syndrome manifestations in children born after in vitro fertilization.
    Fertil Steril. 2010 Oct;94(5):1693-9 PMID: 20045517
  164. Assisted reproduction treatment and epigenetic inheritance.
    Hum Reprod Update. 2012 Mar-Apr;18(2):171-97 PMID: 22267841
  165. Epigenetic programming and risk: the birthplace of cardiovascular disease?
    Stem Cell Rev. 2013 Jun;9(3):241-53 PMID: 22773406
  166. From endothelial dysfunction to atherosclerosis.
    Autoimmun Rev. 2010 Oct;9(12):830-4 PMID: 20678595
  167. Neuronatin: a new inflammation gene expressed on the aortic endothelium of diabetic mice.
    Diabetes. 2008 Oct;57(10):2774-83 PMID: 18591389
  168. Incidence of retinoblastoma in children born after in-vitro fertilisation.
    Lancet. 2003 Jan 25;361(9354):309-10 PMID: 12559867
  169. Outcome of assisted reproduction.
    Lancet. 2007 Jul 28;370(9584):351-9 PMID: 17662884
  170. Zygotic gene activation and maternal factors in mammals.
    J Reprod Dev. 2007 Aug;53(4):707-15 PMID: 17827882
  171. Epigenetics in human disease and prospects for epigenetic therapy.
    Nature. 2004 May 27;429(6990):457-63 PMID: 15164071
  172. The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization.
    N Engl J Med. 2002 Mar 7;346(10):725-30 PMID: 11882727
  173. Growth and maturation of cardiac myocytes in fetal sheep in the second half of gestation.
    Anat Rec A Discov Mol Cell Evol Biol. 2003 Oct;274(2):952-61 PMID: 12973719
  174. Formation of the ovarian follicular antrum and follicular fluid.
    Biol Reprod. 2010 Jun;82(6):1021-9 PMID: 20164441
  175. The impact of ovarian stimulation on the expression of candidate reprogramming genes in mouse preimplantation embryos.
    Cytogenet Genome Res. 2013;139(2):71-9 PMID: 23154201
  176. The longer-term health outcomes for children born as a result of IVF treatment: Part I--General health outcomes.
    Hum Reprod Update. 2013 May-Jun;19(3):232-43 PMID: 23449642
  177. A persistent misperception: assisted reproductive technology can reverse the "aged biological clock".
    Fertil Steril. 2012 May;97(5):1044-7 PMID: 22386844
  178. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status.
    Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19351-6 PMID: 18042717
  179. Manipulating nature: Might there be a cardiovascular price to pay for the miracle of assisted conception?
    Circulation. 2012 Apr 17;125(15):1832-4 PMID: 22434594
  180. Histone modifications during mammalian oocyte maturation: dynamics, regulation and functions.
    Cell Cycle. 2010 May 15;9(10):1942-50 PMID: 20436284
  181. GIFT, ZIFT, and related techniques.
    Curr Opin Obstet Gynecol. 1993 Oct;5(5):615-22 PMID: 8241437
  182. Demethylation of the zygotic paternal genome.
    Nature. 2000 Feb 3;403(6769):501-2 PMID: 10676950
  183. Low and very low birth weight in infants conceived with use of assisted reproductive technology.
    N Engl J Med. 2002 Mar 7;346(10):731-7 PMID: 11882728
  184. Pregnancy outcomes after assisted reproductive technology.
    J Obstet Gynaecol Can. 2006 Mar;28(3):220-50 PMID: 16650361
  185. Zona pellucida glycoproteins.
    Annu Rev Biochem. 1988;57:415-42 PMID: 3052278
  186. Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease.
    Biol Reprod. 2008 Feb;78(2):299-306 PMID: 17989357
  187. A methyl-deficient diet fed to rats during the pre- and peri-conception periods of development modifies the hepatic proteome in the adult offspring.
    Genes Nutr. 2013 Mar;8(2):181-90 PMID: 22907820
  188. Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner.
    Hum Mol Genet. 2010 Jan 1;19(1):36-51 PMID: 19805400
  189. Peri-implantation hormonal milieu: elucidating mechanisms of abnormal placentation and fetal growth.
    Biol Reprod. 2014 Feb;90(2):26 PMID: 24352558
  190. The antral follicle: a microenvironment for oocyte differentiation.
    Int J Dev Biol. 2012;56(10-12):819-31 PMID: 23417404
  191. Large offspring syndrome and other consequences of ruminant embryo culture in vitro: relevance to blastocyst culture in human ART.
    Hum Fertil (Camb). 2000;3(4):238-246 PMID: 11844385
  192. Beckwith-Wiedemann syndrome and assisted reproduction technology (ART).
    J Med Genet. 2003 Jan;40(1):62-4 PMID: 12525545
  193. Maternal nutrition at conception modulates DNA methylation of human metastable epialleles.
    Nat Commun. 2014;5:3746 PMID: 24781383
  194. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming.
    Physiol Rev. 2005 Apr;85(2):571-633 PMID: 15788706
  195. Gamete intrafallopian transfer. International cooperative study of the first 800 cases.
    Ann N Y Acad Sci. 1988;541:722-7 PMID: 3195949
  196. Birth after the reimplantation of a human embryo.
    Lancet. 1978 Aug 12;2(8085):366 PMID: 79723
  197. Cardiometabolic differences in children born after in vitro fertilization: follow-up study.
    J Clin Endocrinol Metab. 2008 May;93(5):1682-8 PMID: 18285409
  198. The Dutch famine and its long-term consequences for adult health.
    Early Hum Dev. 2006 Aug;82(8):485-91 PMID: 16876341
  199. Aberrant methylation patterns at the two-cell stage as an indicator of early developmental failure.
    Mol Reprod Dev. 2002 Nov;63(3):329-34 PMID: 12237948
  200. Assisted reproductive technology after the birth of louise brown.
    J Reprod Infertil. 2013 Jul;14(3):96-109 PMID: 24163793
  201. Cardiac myocyte cell cycle control in development, disease, and regeneration.
    Physiol Rev. 2007 Apr;87(2):521-44 PMID: 17429040
  202. Implantation mechanisms: insights from the sheep.
    Reproduction. 2004 Dec;128(6):657-68 PMID: 15579583
  203. Eight-fold increased risk for congenital heart defects in children carrying the nicotinamide N-methyltransferase polymorphism and exposed to medicines and low nicotinamide.
    Eur Heart J. 2008 Jun;29(11):1424-31 PMID: 18441319
  204. Vascular dysfunction in children conceived by assisted reproductive technologies: underlying mechanisms and future implications.
    Swiss Med Wkly. 2014;144:w13973 PMID: 24964004
  205. Insulin sensitivity is normalized in the third generation (F3) offspring of developmentally programmed insulin resistant (F2) rats fed an energy-restricted diet.
    Nutr Metab (Lond). 2008 Oct 17;5:26 PMID: 18928547
  206. Long-term outcomes in children born after assisted conception.
    Semin Reprod Med. 2012 Apr;30(2):123-30 PMID: 22549712
  207. Investigation of the infertile couple: investigation of the infertile couple in the era of assisted reproductive technology: a time for reappraisal.
    Hum Reprod. 2000 Nov;15(11):2251-7 PMID: 11056115
  208. The International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) Revised Glossary on ART Terminology, 2009.
    Hum Reprod. 2009 Nov;24(11):2683-7 PMID: 19801627
  209. Zygote donor nitrogen metabolism and in vitro embryo culture perturbs in utero development and IGF2R expression in ovine fetal tissues.
    Theriogenology. 2006 Nov;66(8):1901-12 PMID: 16777210
  210. A comprehensive assessment of outcomes in pregnancies conceived by in vitro fertilization/intracytoplasmic sperm injection.
    Eur J Obstet Gynecol Reprod Biol. 2010 Jun;150(2):160-5 PMID: 20207067
  211. Gamete intrafallopian transfer.
    Vet Clin North Am Equine Pract. 1996 Apr;12(1):47-60 PMID: 8726449
  212. Pregnancy recognition and conceptus implantation in domestic ruminants: roles of progesterone, interferons and endogenous retroviruses.
    Reprod Fertil Dev. 2007;19(1):65-78 PMID: 17389136
  213. Carotid intima-media thickness, arterial stiffness and risk of cardiovascular disease: current evidence.
    J Hypertens. 2002 Dec;20(12):2317-25 PMID: 12473847
  214. Molecular mechanisms of epigenetics.
    Biochemistry (Mosc). 2005 Apr;70(4):406-23 PMID: 15892607
  215. Changes with age in the level and duration of fertility in the menstrual cycle.
    Hum Reprod. 2002 May;17(5):1399-403 PMID: 11980771
  216. Large offspring syndrome in cattle and sheep.
    Rev Reprod. 1998 Sep;3(3):155-63 PMID: 9829550
  217. Cardiomyocytes structure, function and associated pathologies.
    Int J Biochem Cell Biol. 2005 Sep;37(9):1746-51 PMID: 15950518
  218. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases.
    Nat Rev Endocrinol. 2009 Jul;5(7):401-8 PMID: 19488075
  219. Impact of periconceptional nutrition on maternal and fetal leptin and fetal adiposity in singleton and twin pregnancies.
    Am J Physiol Regul Integr Comp Physiol. 2005 Jan;288(1):R39-45 PMID: 15191901
  220. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line.
    Genes Dev. 1992 May;6(5):705-14 PMID: 1577268
  221. Growth and development of children born after in vitro fertilization.
    Fertil Steril. 2008 Nov;90(5):1662-73 PMID: 18163998
  222. Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure.
    Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5449-54 PMID: 17372207
  223. Myocardial cell hypertrophy or hyperplasia.
    Hypertension. 1984 Nov-Dec;6(6 Pt 2):III38-43 PMID: 6240451
  224. Persistent epigenetic differences associated with prenatal exposure to famine in humans.
    Proc Natl Acad Sci U S A. 2008 Nov 4;105(44):17046-9 PMID: 18955703
  225. Gamete intrafallopian transfer.
    Br J Hosp Med. 1996 Apr 17-30;55(8):468-71 PMID: 8732214
  226. Assisted reproductive technology and major structural birth defects in the United States.
    Hum Reprod. 2009 Feb;24(2):360-6 PMID: 19010807
  227. Ovulation induction and epigenetic anomalies.
    Fertil Steril. 2013 Mar 1;99(3):616-23 PMID: 23714436
  228. The double hit of growth restriction: its origins and outcome on this generation and the next.
    J Physiol. 2012 Mar 1;590(Pt 5):1019 PMID: 22399819
  229. CCAAT/enhancer binding protein alpha (C/EBPalpha) in adipose tissue regulates genes in lipid and glucose metabolism and a genetic variation in C/EBPalpha is associated with serum levels of triglycerides.
    J Clin Endocrinol Metab. 2008 Dec;93(12):4880-6 PMID: 18765514
  230. Single embryo transfer and multiple pregnancy rate reduction in IVF/ICSI: a 5-year appraisal.
    Reprod Biomed Online. 2003 Jun;6(4):464-9 PMID: 12831596
  231. Can assisted reproduction technology compensate for the natural decline in fertility with age? A model assessment.
    Hum Reprod. 2004 Jul;19(7):1548-53 PMID: 15205397
  232. Does in vitro fertilisation increase type 2 diabetes and cardiovascular risk?
    Curr Diabetes Rev. 2011 Nov;7(6):426-32 PMID: 22091747
  233. Transient regenerative potential of the neonatal mouse heart.
    Science. 2011 Feb 25;331(6020):1078-80 PMID: 21350179
  234. Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamo-pituitary adrenal axis in sheep during late gestation.
    Biol Reprod. 2002 May;66(5):1562-9 PMID: 11967224
  235. Initial and cyclic recruitment of ovarian follicles.
    Endocr Rev. 2000 Apr;21(2):200-14 PMID: 10782364
  236. The effect of oocyte quality on development.
    J Anim Sci. 2004;82 E-Suppl:E14-23 PMID: 15471793
  237. Genomic imprinting: review and relevance to human diseases.
    Am J Hum Genet. 1990 May;46(5):857-73 PMID: 2187341
  238. Lamb birth weight is affected by culture system utilized during in vitro pre-elongation development of ovine embryos.
    Biol Reprod. 1995 Dec;53(6):1385-91 PMID: 8562695
  239. Early origins of heart disease: low birth weight and determinants of cardiomyocyte endowment.
    Clin Exp Pharmacol Physiol. 2012 Sep;39(9):814-23 PMID: 22126336
  240. Periconceptional tobacco smoking and isolated congenital heart defects in the neonatal period.
    Int J Cardiol. 2011 May 5;148(3):295-9 PMID: 19951824
  241. Formation of binucleated myocardial cells in the neonatal rat. An index for growth hypertrophy.
    Lab Invest. 1984 May;50(5):571-7 PMID: 6232423
  242. The genomics of the human endometrium.
    Biochim Biophys Acta. 2012 Dec;1822(12):1931-42 PMID: 22634130
  243. Zygote intra-fallopian transfer as an alternative treatment for male infertility.
    Hum Reprod. 1989 May;4(4):412-5 PMID: 2745671
  244. IVF results: optimize not maximize.
    Am J Obstet Gynecol. 2006 Feb;194(2):322-31 PMID: 16458624
  245. Congenital malformations associated with assisted reproductive technology: a California statewide analysis.
    J Pediatr Surg. 2013 Jun;48(6):1218-24 PMID: 23845610
  246. Childhood origins of arterial disease.
    Curr Opin Pediatr. 2007 Oct;19(5):538-45 PMID: 17885471
  247. In vitro fertilization causes epigenetic modifications to the onset of gene expression from the zygotic genome in mice.
    Biol Reprod. 2001 Feb;64(2):696-705 PMID: 11159375
  248. Reproductive technologies and the risk of birth defects.
    N Engl J Med. 2012 May 10;366(19):1803-13 PMID: 22559061
  249. Noninvasive assessment of subclinical atherosclerosis in children and adolescents: recommendations for standard assessment for clinical research: a scientific statement from the American Heart Association.
    Hypertension. 2009 Nov;54(5):919-50 PMID: 19729599
  250. Post-natal growth and development of Simmental calves derived from in vivo or in vitro embryos.
    Reprod Fertil Dev. 1998;10(6):459-64 PMID: 10588375
  251. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19.
    Am J Hum Genet. 2003 Jan;72(1):156-60 PMID: 12439823
  252. Prevention of congenital abnormalities by periconceptional multivitamin supplementation.
    BMJ. 1993 Jun 19;306(6893):1645-8 PMID: 8324432
  253. Trends in the incidence of births and multiple births and the factors that determine the probability of multiple birth after IVF treatment.
    Hum Reprod. 2001 Dec;16(12):2598-605 PMID: 11726581
  254. Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep.
    Hypertension. 2004 Jun;43(6):1290-6 PMID: 15078864
  255. Comparison of Congenital Abnormalities of Infants Conceived by Assisted Reproductive Techniques versus Infants with Natural Conception in Tehran.
    Int J Fertil Steril. 2013 Oct;7(3):217-24 PMID: 24520489
Article Info
Journal
Nutrients
Abbr.
Nutrients
ISSN
2072-6643
Published
2015-02-18
Epub
2015-00-18
Pages
1378-425
Language
English
Region
Switzerland
NLM ID
101521595
PMCID
PMC4377860
Subset
IM
Analysis Services
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