Cardiovascular and metabolic profiles of offspring conceived by assisted reproductive technologies: a systematic review and meta-analysis

Fertility and Sterility

Volumn 107, Issue 3, 2017, Pages 622-631.e5

  Guo, Xiao Yan ^a   Liu, Xin Mei ^b   Jin, Li ^b   Wang, Ting Ting ^b   Ullah, Kamran ^c   Sheng, Jian Zhong ^c   Huang, He Feng ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

blood pressure; BMI; ICSI; IVF; metabolism

Indexed keywords

GLUCOSE; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; BIOLOGICAL MARKER; INSULIN;

ARTICLE; BLOOD VESSEL WALL; BODY MASS; CARDIOVASCULAR FUNCTION; CHOLESTEROL BLOOD LEVEL; CLINICAL FEATURE; CRYOPRESERVATION; DIASTOLIC BLOOD PRESSURE; GLUCOSE HOMEOSTASIS; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; LIFESTYLE; LIPID METABOLISM; MEDLINE; META ANALYSIS; METABOLIC PARAMETERS; METABOLISM; OBESITY; PRIORITY JOURNAL; PROGENY; SCOPUS; SYSTEMATIC REVIEW; SYSTOLIC BLOOD PRESSURE; ADOLESCENT; AGE; BLOOD; BLOOD PRESSURE; CHILD; DYSLIPIDEMIA; FEMALE; GLUCOSE BLOOD LEVEL; HYPERTENSION; INFANT; INFERTILITY; INFERTILITY THERAPY; INSULIN RESISTANCE; LIVE BIRTH; PATHOPHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; PRESCHOOL CHILD; RISK ASSESSMENT; RISK FACTOR; TREATMENT OUTCOME; YOUNG ADULT;

ADIPOSITY; ADOLESCENT; AGE FACTORS; BIOMARKERS; BLOOD GLUCOSE; BLOOD PRESSURE; BODY MASS INDEX; CHILD; CHILD, PRESCHOOL; DYSLIPIDEMIAS; FEMALE; HUMANS; HYPERTENSION; INFANT; INFERTILITY; INSULIN; INSULIN RESISTANCE; LIPIDS; LIVE BIRTH; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REPRODUCTIVE TECHNIQUES, ASSISTED; RISK ASSESSMENT; RISK FACTORS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 85009414562     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2016.12.007     Document Type: Article

References (105)

1. 1 Kissin, D.M., Jamieson, D.J., Barfield, W.D., Monitoring health outcomes of assisted reproductive technology. New Engl J Med 371 (2014), 91–93.
2. 2 Reik, W., Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447 (2007), 425–432.
3. 3 Feil, R., Fraga, M.F., Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 13 (2012), 97–109.
4. 4 Niakan, K.K., Han, J., Pedersen, R.A., Simon, C., Pera, R.A., Human pre-implantation embryo development. Development 139 (2012), 829–841.
5. 5 Romundstad, L.B., Romundstad, P.R., Sunde, A., von Düring, V., Skjærven, R., Gunnell, D., et al. Effects of technology or maternal factors on perinatal outcome after assisted fertilisation: a population-based cohort study. Lancet 372 (2008), 737–743.
6. 6 Hansen, M., Kurinczuk, J.J., Milne, E., de Klerk, N., Bower, C., Assisted reproductive technology and birth defects: a systematic review and meta-analysis. Hum Reprod Update 19 (2013), 330–353.
7. 7 Pinborg, A., Wennerholm, U.B., Romundstad, L.B., Loft, A., Aittomaki, K., Sö derström-Anttila, V., et al. Why do singletons conceived after assisted reproduction technology have adverse perinatal outcome? Systematic review and meta-analysis. Hum Reprod Update 19 (2013), 87–104.
8. 8 Barker, D.J., Osmond, C., Golding, J., Kuh, D., Wadsworth, M.E., Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 298 (1989), 564–567.
9. 9 Barker, D.J., The origins of the developmental origins theory. J Intern Med 261 (2007), 412–417.
10. 10 Morton, J.S., Cooke, C.L., Davidge, S.T., In utero origins of hypertension: mechanisms and targets for therapy. Physiol Rev 96 (2016), 549–603.
11. 11 Rexhaj, E., Paoloni-Giacobino, A., Rimoldi, S.F., Fuster, D.G., Anderegg, M., Somm, E., et al. Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span. J Clin Invest 123 (2013), 5052–5060.
12. 12 Schenewerk, A.L., Ramírez, F.Í., Foote, C., Ji, T., Martínez-Lemus, L.A., Rivera, R.M., Effects of the use of assisted reproduction and high-caloric diet consumption on body weight and cardiovascular health of juvenile mouse offspring. Reproduction 147 (2014), 111–123.
13. 13 Watkins, A.J., Platt, D., Papenbrock, T., Wilkins, A., Eckert, J.J., Wing, Y.K., et al. Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure. Proc Natl Acad Sci USA 104 (2007), 5449–5454.
14. 14 Rexhaj, E., Pireva, A., Paoloni-Giacobino, A., Allemann, Y., Cerny, D., Dessen, P., et al. Prevention of vascular dysfunction and arterial hypertension in mice generated by assisted reproductive technologies by addition of melatonin to culture media. Am J Physiol Heart Circ Physiol 309 (2015), H1151–H1156.
15. 15 Scott, K.A., Yamazaki, Y., Yamamoto, M., Lin, Y., Melhorn, S.J., Krause, E.G., et al. Glucose parameters are altered in mouse offspring produced by assisted reproductive technologies and somatic cell nuclear transfer. Biol Reprod 83 (2010), 220–227.
16. 16 Donjacour, A., Liu, X., Lin, W., Simbulan, R., Rinaudo, P.F., In vitro fertilization affects growth and glucose metabolism in a sex-specific manner in an outbred mouse model. Biol Reprod, 90, 2014, 80.
17. 17 Wang, L.Y., Le, F., Wang, N., Li, L., Liu, X.Z., Zheng, Y.M., et al. Alteration of fatty acid metabolism in the liver, adipose tissue, and testis of male mice conceived through assisted reproductive technologies: fatty acid metabolism in ART mice. Lipids Health Dis, 12, 2013, 5.
18. 18 Yeung, E.H., Druschel, C., Cardiometabolic health of children conceived by assisted reproductive technologies. Fertil Steril 99 (2013), 318–326.e4.
19. 19 Scherrer, U., Rexhaj, E., Allemann, Y., Sartori, C., Rimoldi, S.F., Cardiovascular dysfunction in children conceived by assisted reproductive technologies. Eur Heart J 36 (2015), 1583–1589.
20. 20 Wikstrand, M.H., Niklasson, A., Strömland, K., Hellström, A., Abnormal vessel morphology in boys born after intracytoplasmic sperm injection. Acta Paediatr 97 (2008), 1512–1517.
21. 21 Padhee, M., Zhang, S., Lie, S., Wang, K.C., Botting, K.J., Caroline McMillen, I., et al. The periconceptional environment and cardiovascular disease: Does in vitro embryo culture and transfer influence cardiovascular development and health?. Nutrients 7 (2015), 1378–1425.
22. 22 Gao, Q., Pan, H.T., Lin, X.H., Zhang, J.Y., Jiang, Y., Tian, S., et al. Altered protein expression profiles in umbilical veins: insights into vascular dysfunctions of the children born after in vitro fertilization. Biol Reprod, 91, 2014, 71.
23. 23 Johansson, S., Iliadou, A., Bergvall, N., Tuvemo, T., Norman, M., Cnattingius, S., Risk of high blood pressure among young men increases with the degree of immaturity at birth. Circulation 112 (2005), 3430–3436.
24. 24 Kaijser, M., Bonamy, A.K., Akre, O., Cnattingius, S., Granath, F., Norman, M., et al. Perinatal risk factors for ischemic heart disease: Disentangling the roles of birth weight and preterm birth. Circulation 117 (2008), 405–410.
25. 25 De Jong, F., Monuteaux, M.C., Van Elburg, R.M., Gillman, M.W., Belfort, M.B., Systematic review and meta-analysis of preterm birth and later systolic blood pressure. Hypertension 59 (2012), 226–234.
26. 26 Bay, B., Mortensen, E.L., Kesmodel, U.S., Is subfertility or fertility treatment associated with long-term growth in the offspring? A cohort study. Fertil Steril 102 (2014), 1117–1123.
27. 27 Xu, G.F., Zhang, J.Y., Pan, H.T., Tian, S., Liu, M.E., Yu, T.T., et al. Cardiovascular dysfunction in offspring of ovarian-hyperstimulated women and effects of estradiol and progesterone: a retrospective cohort study and proteomics analysis. J Clin Endocrinol Metab 99 (2014), E2494–E2503.
28. 28 Seggers, J., Haadsma, M.L., Bastide-Van Gemert, S.L., Heineman, M.J., Kok, J.H., Middelburg, K.J., et al. Blood pressure and anthropometrics of 4-y-old children born after preimplantation genetic screening: Follow-up of a unique, moderately sized, randomized controlled trial. Pediatr Res 74 (2013), 606–614.
29. 29 Bouillon, C., Leandri, R., Desch, L., Ernst, A., Bruno, C., Cerf, C., et al. Does embryo culture medium influence the health and development of children born after in vitro fertilization?. PLoS One, 11, 2016, e0150857.
30. 30 Desmyttere, S., Bonduelle, M., Nekkebroeck, J., Roelants, M., Liebaers, I., De Schepper, J., Growth and health outcome of 102 2-year-old children conceived after preimplantation genetic diagnosis or screening. Early Hum Dev 85 (2009), 755–759.
31. 31 Wennerholm, U.B., Bonduelle, M., Sutcliffe, A., Bergh, C., Niklasson, A., Tarlatzis, B., et al. Paternal sperm concentration and growth and cognitive development in children born with a gestational age more than 32 weeks after assisted reproductive therapy. Hum Reprod 21 (2006), 1514–1520.
32. 32 Foix-L'Helias, L., Grynberg, M., Ducot, B., Frydman, N., Kerbrat, V., Bouyer, J., et al. Growth development of French children born after in vitro maturation. PLoS One, 9, 2014, e89713.
33. 33 Belva, F., Painter, R., Bonduelle, M., Roelants, M., Devroey, P., De Schepper, J., Are ICSI adolescents at risk for increased adiposity?. Hum Reprod 27 (2012), 257–264.
34. 34 Belva, F., Roelants, M., Painter, R., Bonduelle, M., Devroey, P., De Schepper, J., Pubertal development in ICSI children. Hum Reprod 27 (2012), 1156–1161.
35. 35 Ceelen, M., Van Weissenbruch, M.M., Roos, J.C., Vermeiden, J.P., Van Leeuwen, F.E., Delemarre-van De Waal, H.A., Body composition in children and adolescents born after in vitro fertilization or spontaneous conception. J Clin Endocrinol Metab 92 (2007), 3417–3423.
36. 36 Ceelen, M., Van Weissenbruch, M.M., Vermeiden, J.P.W., Van Leeuwen, F.E., Delemarre-Van De Waal, H.A., Pubertal development in children and adolescents born after IVF and spontaneous conception. Hum Reprod 23 (2008), 2791–2798.
37. 37 Ceelen, M., Van Weissenbruch, M.M., Prein, J., Smit, J.J., Vermeiden, J.P., Spreeuwenberg, M., et al. 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 24 (2009), 2788–2795.
38. 38 Miles, H.L., Hofman, P.L., Peek, J., Harris, M., Wilson, D., Robinson, E.M., et al. In vitro fertilization improves childhood growth and metabolism. J Clin Endocrinol Metab 92 (2007), 3441–3445.
39. 39 Sakka, S.D., Margeli, A., Loutradis, D., Chrousos, G.P., Papassotiriou, I., Kanaka-Gantenbein, C., Gender dimorphic increase in RBP-4 and NGAL in children born after IVF: an epigenetic phenomenon?. Eur J Clin Invest 43 (2013), 439–448.
40. 40 Rimoldi, S.F., Sartori, C., Rexhaj, E., Bailey, D.M., Marchi, S.F., McEneny, J., et al. Antioxidants improve vascular function in children conceived by assisted reproductive technologies: a randomized double-blind placebo-controlled trial. Eur J Prev Cardiol 22 (2015), 1399–1407.
41. 41 Beydoun, H.A., Sicignano, N., Beydoun, M.A., Matson, D.O., Bocca, S., Stadtmauer, L., et al. A cross-sectional evaluation of the first cohort of young adults conceived by in vitro fertilization in the United States. Fertil Steril 94 (2010), 2043–2049.
42. 42 Beydoun, H.A., Sicignano, N., Beydoun, M.A., Bocca, S., Stadtmauer, L., Oehninger, S., Pubertal development of the first cohort of young adults conceived by in vitro fertilization in the United States. Fertil Steril 95 (2011), 528–533.
43. 43 Bonduelle, M., Bergh, C., Niklasson, A., Palermo, G.D., Wennerholm, U.B., Collaborative Study Group B. Medical follow-up study of 5-year-old ICSI children. Reprod Biomed Online 9 (2004), 91–101.
44. 44 Belva, F., Henriet, S., Liebaers, I., Van Steirteghem, A., Celestin-Westreich, S., Bonduelle, M., Medical outcome of 8-year-old singleton ICSI children (born ≥32 weeks’ gestation) and a spontaneously conceived comparison group. Hum Reprod 22 (2007), 506–515.
45. 45 Chen, M., Wu, L., Zhao, J., Wu, F., Davies, M.J., Wittert, G.A., et al. Altered glucose metabolism in mouse and humans conceived by IVF. Diabetes 63 (2014), 3189–3198.
46. 46 Scherrer, U., Rimoldi, S.F., Rexhaj, E., Stuber, T., Duplain, H., Garcin, S., et al. Systemic and pulmonary vascular dysfunction in children conceived by assisted reproductive technologies. Circulation 125 (2012), 1890–1896.
47. 47 Belva, F., Roelants, M., De Schepper, J., Roseboom, T.J., Bonduelle, M., Devroey, P., et al. Blood pressure in ICSI-conceived adolescents. Hum Reprod 27 (2012), 3100–3108.
48. 48 Ceelen, M., van Weissenbruch, M.M., Vermeiden, J.P., van Leeuwen, F.E., Delemarre-van de Waal, H.A., Cardiometabolic differences in children born after in vitro fertilization: follow-up study. J Clin Endocrinol Metab 93 (2008), 1682–1688.
49. 49 Desmyttere, S., De Schepper, J., Nekkebroeck, J., De Vos, A., De Rycke, M., Staessen, C., et al. Two-year auxological and medical outcome of singletons born after embryo biopsy applied in preimplantation genetic diagnosis or preimplantation genetic screening. Hum Reprod 24 (2009), 470–476.
50. 50 Gkourogianni, A., Kosteria, I., Telonis, A.G., Margeli, A., Mantzou, E., Konsta, M., et al. Plasma metabolomic profiling suggests early indications for predisposition to latent insulin resistance in children conceived by ICSI. PLoS One, 9, 2014, e94001.
51. 51 Green, M.P., Mouat, F., Miles, H.L., Hopkins, S.A., Derraik, J.G., Hofman, P.L., et al. Phenotypic differences in children conceived from fresh and thawed embryos in in vitro fertilization compared with naturally conceived children. Fertil Steril 99 (2013), 1898–1904.
52. 52 Halliday, J., Wilson, C., Hammarberg, K., Doyle, L.W., Bruinsma, F., McLachlan, R., et al. Comparing indicators of health and development of singleton young adults conceived with and without assisted reproductive technology. Fertil Steril 101 (2014), 1055–1063.
53. 53 Kai, C.M., Main, K.M., Andersen, A.N., Loft, A., Chellakooty, M., Skakkebæk, N.E., et al. Serum insulin-like growth factor-I (IGF-I) and growth in children born after assisted reproduction. J Clin Endocrinol Metab 91 (2006), 4352–4360.
54. 54 Knoester, M., Helmerhorst, F.M., Vandenbroucke, J.P., van der Westerlaken, L.A., Walther, F.J., Veen, S., Perinatal outcome, health, growth, and medical care utilization of 5- to 8-year-old intracytoplasmic sperm injection singletons. Fertil Steril 89 (2008), 1133–1146.
55. 55 Liu, H., Zhang, Y., Gu, H.T., Feng, Q.L., Liu, J.Y., Zhou, J., et al. Association between assisted reproductive technology and cardiac alteration at age 5 years. JAMA Pediatr 169 (2015), 603–605.
56. 56 Ludwig, A.K., Katalinic, A., Thyen, U., Sutcliffe, A.G., Diedrich, K., Ludwig, M., Physical health at 5.5 years of age of term-born singletons after intracytoplasmic sperm injection: results of a prospective, controlled, single-blinded study. Fertil Steril 91 (2009), 115–124.
57. 57 Pontesilli, M., Painter, R.C., Grooten, I.J., Van Der Post, J.A., Mol, B.W., Vrijkotte, T.G., et al. Subfertility and assisted reproduction techniques are associated with poorer cardiometabolic profiles in childhood. Reprod Biomed Online 30 (2015), 258–267.
58. 58 Sakka, S.D., Loutradis, D., Kanaka-Gantenbein, C., Margeli, A., Papastamataki, M., Papassotiriou, I., et al. Absence of insulin resistance and low-grade inflammation despite early metabolic syndrome manifestations in children born after in vitro fertilization. Fertil Steril 94 (2010), 1693–1699.
59. 59 Seggers, J., Haadsma, M.L., La Bastide-Van Gemert, S., Heineman, M.J., Middelburg, K.J., Roseboom, T.J., et al. Is ovarian hyperstimulation associated with higher blood pressure in 4-year-old IVF offspring? Part I: multivariable regression analysis. Hum Reprod 29 (2014), 502–509.
60. 60 Valenzuela-Alcaraz, B., Crispi, F., Bijnens, B., Cruz-Lemini, M., Creus, M., Sitges, M., et al. Assisted reproductive technologies are associated with cardiovascular remodeling in utero that persists postnatally. Circulation 128 (2013), 1442–1450.
61. 61 Von Arx, R., Allemann, Y., Sartori, C., Rexhaj, E., Cerny, D., de Marchi, S.F., et al. Right ventricular dysfunction in children and adolescents conceived by assisted reproductive technologies. J Appl Physiol 118 (2015), 1200–1206.
62. 62 Zhou, J., Liu, H., Gu, H.T., Cui, Y.G., Zhao, N.N., Chen, J., et al. Association of cardiac development with assisted reproductive technology in childhood: a prospective single-blind pilot study. Cell Physiol Biochem 34 (2014), 988–1000.
63. 63 Stang, A., Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25 (2010), 603–605.
64. 64 Borenstein, M., Hedges, L.V., Higgins, J.P., Rothstein, H.R., Introduction to meta-analysis. 2009, John Wiley & Sons, Chichester, United Kingdom.
65. 65 Hickman, T.B., Briefel, R.R., Carroll, M.D., Rifkind, B.M., Cleeman, J.I., Maurer, K.R., et al. Distributions and trends of serum lipid levels among United States children and adolescents ages 4–19 years: data from the Third National Health and Nutrition Examination Survey. Prev Med 27 (1998), 879–890.
66. 66 National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents. The Fourth Report on the Diagnosis, Evaluation, and Treatment of High Blood Pressure in Children and Adolescents. Pediatrics 114 (2004), 555–576.
67. 67 Wang, J., Sauer, M.V., In vitro fertilization (IVF): a review of 3 decades of clinical innovation and technological advancement. Ther Clin Risk Manag 2 (2006), 355–364.
68. 68 Boulet, S.L., Mehta, A., Kissin, D.M., Warner, L., Kawwass, J.F., Jamieson, D.J., Trends in use of and reproductive outcomes associated with intracytoplasmic sperm injection. JAMA 313 (2015), 255–263.
69. 69 Law, C.M., De Swiet, M., Osmond, C., Fayers, P.M., Barker, D.J.P., Cruddas, A.M., et al. Initiation of hypertension in utero and its amplification throughout life. BMJ 306 (1992), 24–27.
70. 70 Srinivasan, S.R., Myers, L., Berenson, G.S., Changes in metabolic syndrome variables since childhood in prehypertensive and hypertensive subjects: the Bogalusa Heart Study. Hypertension 48 (2006), 33–39.
71. 71 Chen, X., Wang, Y., Tracking of blood pressure from childhood to adulthood: a systematic review and meta-regression analysis. Circulation 117 (2008), 3171–3180.
72. 72 Rademacher, E.R., Jacobs, D.R. Jr., Moran, A., Steinberger, J., Prineas, R.J., Sinaiko, A., Relation of blood pressure and body mass index during childhood to cardiovascular risk factor levels in young adults. J Hypertens 27 (2009), 1766–1774.
73. 73 Morrison, J.A., Glueck, C.J., Wang, P., Childhood risk factors predict cardiovascular disease, impaired fasting glucose plus type 2 diabetes mellitus, and high blood pressure 26 years later at a mean age of 38 years: the Princeton-lipid research clinics follow-up study. Metabolism 61 (2012), 531–541.
74. 74 Whelton, P.K., He, J., Appel, L.J., Cutler, J.A., Havas, S., Kotchen, T.A., et al. Primary prevention of hypertension: clinical and public health advisory from the National High Blood Pressure Education Program. JAMA 288 (2002), 1882–1888.
75. 75 Cook, N.R., Cohen, J., Hebert, P.R., Taylor, J.O., Hennekens, C.H., Implications of small reductions in diastolic blood pressure for primary prevention. Arch Intern Med 155 (1995), 701–709.
76. 76 Kallen, B., Finnstrom, O., Lindam, A., Nilsson, E., Nygren, K.G., Otterblad Olausson, P., Trends in delivery and neonatal outcome after in vitro fertilization in Sweden: data for 25 years. Hum Reprod 25 (2010), 1026–1034.
77. 77 Hansen, M., Kurinczuk, J.J., de Klerk, N., Burton, P., Bower, C., Assisted reproductive technology and major birth defects in Western Australia. Obstet Gynecol 120 (2012), 852–863.
78. 78 Henningsen, A.A., Gissler, M., Skjaerven, R., Bergh, C., Tiitinen, A., Romundstad, L.B., et al. Trends in perinatal health after assisted reproduction: a Nordic study from the CoNARTaS group. Hum Reprod 30 (2015), 710–716.
79. 79 Hart, R., Norman, R.J., The longer-term health outcomes for children born as a result of IVF treatment: Part I—general health outcomes. Hum Reprod Update 19 (2013), 232–243.
80. 80 Zhu, Y.M., Hu, X.L., Wu, Y.T., Feng, C., Huang, H.F., Assisted reproductive technology and gamete/embryo-fetal origins of diseases. Huang, H.F., Sheng, J.Z., (eds.) Gamete and embryo-fetal origins of adult diseases, 2014, Springer, Dordrecht, the Netherlands, 197–219.
81. 81 Hanson, M.A., Gluckman, P.D., Early developmental conditioning of later health and disease: physiology or pathophysiology?. Physiol Rev 94 (2014), 1027–1076.
82. 82 Kobayashi, H., Sato, A., Otsu, E., Hiura, H., Tomatsu, C., Utsunomiya, T., et al. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 16 (2007), 2542–2551.
83. 83 Khoueiry, R., Ibala-Rhomdane, S., Mery, L., Blachere, T., Guerin, J.F., Lornage, J., et al. Dynamic CpG methylation of the KCNQ1OT1 gene during maturation of human oocytes. J Med Genet 45 (2008), 583–588.
84. 84 Aitken, R.J., Curry, B.J., Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid Redox Signal 14 (2011), 367–381.
85. 85 London, S.N., Young, D., Caldito, G., Mailhes, J.B., Clomiphene citrate-induced perturbations during meiotic maturation and cytogenetic abnormalities in mouse oocytes in vivo and in vitro. Fertil Steril 73 (2000), 620–626.
86. 86 Delimitreva, S., Zhivkova, R., Isachenko, E., Umland, N., Nayudu, P.L., Meiotic abnormalities in in vitro-matured marmoset monkey (Callithrix jacchus) oocytes: development of a non-human primate model to investigate causal factors. Hum Reprod 21 (2006), 240–247.
87. 87 Feng, C., Wang, L.Q., Dong, M.Y., Huang, H.F., Assisted reproductive technology may increase clinical mutation detection in male offspring. Fertil Steril 90 (2008), 92–96.
88. 88 Katari, S., Turan, N., Bibikova, M., Erinle, O., Chalian, R., Foster, M., et al. DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet 18 (2009), 3769–3778.
89. 89 Van Montfoort, A.P., Hanssen, L.L., De Sutter, P., Viville, S., Geraedts, J.P., De Boer, P., Assisted reproduction treatment and epigenetic inheritance. Hum Reprod Update 18 (2012), 171–197.
90. 90 Olofsson, L.E., Orho-Melander, M., William-Olsson, L., Sjoholm, K., Sjostrom, L., Groop, L., et al. CCAAT/enhancer binding protein alpha (C/EBPα) in adipose tissue regulates genes in lipid and glucose metabolism and a genetic variation in C/EBPα is associated with serum levels of triglycerides. J Clin Endocrinol Metab 93 (2008), 4880–4886.
91. 91 Feng, C., Tian, S., Zhang, Y., He, J., Zhu, X.M., Zhang, D., et al. General imprinting status is stable in assisted reproduction-conceived offspring. Fertil Steril 96 (2011), 1417–1423.e9.
92. 92 Whitelaw, N., Bhattacharya, S., Hoad, G., Horgan, G.W., Hamilton, M., Haggarty, P., Epigenetic status in the offspring of spontaneous and assisted conception. Hum Reprod 29 (2014), 1452–1458.
93. 93 Vincent, R.N., Gooding, L.D., Louie, K., Chan Wong, E., Ma, S., Altered DNA methylation and expression of PLAGL1 in cord blood from assisted reproductive technology pregnancies compared with natural conceptions. Fertil Steril 106 (2016), 739–748.e3.
94. 94 de Waal, E., Yamazaki, Y., Ingale, P., Bartolomei, M.S., Yanagimachi, R., McCarrey, J.R., Gonadotropin stimulation contributes to an increased incidence of epimutations in ICSI-derived mice. Hum Mol Genet 21 (2012), 4460–4472.
95. 95 Meng, Y., Lv, P.P., Ding, G.L., Yu, T.T., Liu, Y., Shen, Y., et al. High maternal serum estradiol levels induce dyslipidemia in human newborns via a hepatic HMGCR estrogen response element. Sci Rep, 5, 2015, 10086.
96. 96 Roseboom, T., de Rooij, S., Painter, R., The Dutch famine and its long-term consequences for adult health. Early Hum Dev 82 (2006), 485–491.
97. 97 Watkins, A.J., Lucas, E.S., Torrens, C., Cleal, J.K., Green, L., Osmond, C., et al. Maternal low-protein diet during mouse pre-implantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. Br J Nutr 103 (2010), 1762–1770.
98. 98 van Uitert, E.M., Steegers-Theunissen, R.P., Influence of maternal folate status on human fetal growth parameters. Mol Nutr Food Res 57 (2013), 582–595.
99. 99 Weaver, I.C., Cervoni, N., Champagne, F.A., D'Alessio, A.C., Sharma, S., Seckl, J.R., et al. Epigenetic programming by maternal behavior. Nat Neurosci 7 (2004), 847–854.
100. 100 Oberlander, T.F., Weinberg, J., Papsdorf, M., Grunau, R., Misri, S., Devlin, A.M., Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 3 (2008), 97–106.
101. 101 Hart, R.J., Physiological aspects of female fertility: role of the environment, modern lifestyle, and genetics. Physiol Rev 96 (2016), 873–909.
102. 102 Arena, R., Guazzi, M., Lianov, L., Whitsel, L., Berra, K., Lavie, C.J., et al. Healthy lifestyle interventions to combat noncommunicable disease-a novel nonhierarchical connectivity model for key stakeholders: a policy statement from the American Heart Association, European Society of Cardiology, European Association for Cardiovascular Prevention and Rehabilitation, and American College of Preventive Medicine. Eur Heart J 36 (2015), 2097–2109.
103. 103 Banerjee, I., Shevlin, M., Taranissi, M., Thornhill, A., Abdalla, H., Ozturk, O., et al. Health of children conceived after preimplantation genetic diagnosis: a preliminary outcome study. Reprod Biomed Online 16 (2008), 376–381.
104. 104 Hendriks, S., Dancet, E.A., van Pelt, A.M., Hamer, G., Repping, S., Artificial gametes: a systematic review of biological progress towards clinical application. Hum Reprod Update 21 (2015), 285–296.
105. 105 Inhorn, M.C., Patrizio, P., Infertility around the globe: new thinking on gender, reproductive technologies and global movements in the 21st century. Hum Reprod Update 21 (2015), 411–426.