Semin Reprod Med 2018; 36(03/04): 183-194
DOI: 10.1055/s-0038-1675778
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Child Health: Is It Really Assisted Reproductive Technology that We Need to Be Concerned About?

Edwina H. Yeung
1   Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland
,
Keewan Kim
1   Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland
,
Alexandra Purdue-Smithe
1   Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland
,
Griffith Bell
1   Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland
,
Jessica Zolton
2   Program in Reproductive Endocrinology and Gynecology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland
,
Akhgar Ghassabian
3   Department of Pediatrics, New York University School of Medicine, New York
4   Department of Environmental Medicine, New York University School of Medicine, New York, New York
5   Department of Population Health, New York University School of Medicine, New York, New York
,
Yassaman Vafai
1   Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland
,
Sonia L. Robinson
1   Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland
,
Sunni L. Mumford
1   Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland
› Author Affiliations
Further Information

Publication History

Publication Date:
13 March 2019 (online)

Abstract

Concerns remain about the health of children conceived by infertility treatment. Studies to date have predominantly not identified substantial long-term health effects after accounting for plurality, which is reassuring given the increasing numbers of children conceived by infertility treatment worldwide. However, as technological advances in treatment arise, ongoing studies remain critical for monitoring health effects. To study whether the techniques used in infertility treatment cause health differences, however, remains challenging due to identification of an appropriate comparison group, heterogeneous treatment, and confounding by the underlying causes of infertility. In fact, the factors that are associated with underlying infertility, including parental obesity and other specific male and female factors, may be important independent factors to consider. This review will summarize key methodological considerations in studying children conceived by infertility treatment including the evidence of associations between underlying infertility factors and child health.

 
  • References

  • 1 Calhaz-Jorge C, De Geyter C, Kupka MS. , et al; European IVF-Monitoring Consortium (EIM); European Society of Human Reproduction and Embryology (ESHRE). Assisted reproductive technology in Europe, 2013: results generated from European registers by ESHRE. Hum Reprod 2017; 32 (10) 1957-1973
  • 2 Sunderam S, Kissin DM, Crawford SB. , et al. Assisted reproductive technology surveillance - United States, 2015. MMWR Surveill Summ 2018; 67 (03) 1-28
  • 3 Kushnir VA, Barad DH, Albertini DF, Darmon SK, Gleicher N. Systematic review of worldwide trends in assisted reproductive technology 2004-2013. Reprod Biol Endocrinol 2017; 15 (01) 6
  • 4 Schieve LA, Devine O, Boyle CA, Petrini JR, Warner L. Estimation of the contribution of non-assisted reproductive technology ovulation stimulation fertility treatments to US singleton and multiple births. Am J Epidemiol 2009; 170 (11) 1396-1407
  • 5 Zore T, Wang ET. Perinatal and childhood outcomes associated with infertility. Semin Reprod Med 2017; 35 (03) 304-310
  • 6 Yeung EH, Druschel C. Cardiometabolic health of children conceived by assisted reproductive technologies. Fertil Steril 2013; 99 (02) 318-326
  • 7 Yeung EH, Sundaram R, Bell EM. , et al. Examining infertility treatment and early childhood development in the Upstate KIDS Study. JAMA Pediatr 2016; 170 (03) 251-258
  • 8 Yeung EH, Sundaram R, Bell EM. , et al. Infertility treatment and children's longitudinal growth between birth and 3 years of age. Hum Reprod 2016; 31 (07) 1621-1628
  • 9 Rifouna MS, Reus AD, Koning AH. , et al. First trimester trophoblast and placental bed vascular volume measurements in IVF or IVF/ICSI pregnancies. Hum Reprod 2014; 29 (12) 2644-2649
  • 10 Carson C, Redshaw M, Sacker A, Kelly Y, Kurinczuk JJ, Quigley MA. Effects of pregnancy planning, fertility, and assisted reproductive treatment on child behavioral problems at 5 and 7 years: evidence from the Millennium Cohort Study. Fertil Steril 2013; 99 (02) 456-463
  • 11 Carson C, Sacker A, Kelly Y, Redshaw M, Kurinczuk JJ, Quigley MA. Asthma in children born after infertility treatment: findings from the UK Millennium Cohort Study. Hum Reprod 2013; 28 (02) 471-479
  • 12 Liberman RF, Getz KD, Heinke D. , et al. Assisted reproductive technology and birth defects: effects of subfertility and multiple births. Birth Defects Res 2017; 109 (14) 1144-1153
  • 13 Kissin DM, Boulet SL, Jamieson DJ. ; Assisted Reproductive Technology Surveillance and Research Team. Surveillance ftART, Team R. Fertility treatments in the United States: improving access and outcomes. Obstet Gynecol 2016; 128 (02) 387-390
  • 14 Jain T. Socioeconomic and racial disparities among infertility patients seeking care. Fertil Steril 2006; 85 (04) 876-881
  • 15 Davidovitch M, Chodick G, Shalev V. , et al. Infertility treatments during pregnancy and the risk of autism spectrum disorder in the offspring. Prog Neuropsychopharmacol Biol Psychiatry 2018; 86: 175-179
  • 16 Boulet SL, Mehta A, Kissin DM, Warner L, Kawwass JF, Jamieson DJ. Trends in use of and reproductive outcomes associated with intracytoplasmic sperm injection. JAMA 2015; 313 (03) 255-263
  • 17 Rimm AA, Katayama AC, Diaz M, Katayama KP. A meta-analysis of controlled studies comparing major malformation rates in IVF and ICSI infants with naturally conceived children. J Assist Reprod Genet 2004; 21 (12) 437-443
  • 18 Bonduelle M, Wennerholm UB, Loft A. , et al. A multi-centre cohort study of the physical health of 5-year-old children conceived after intracytoplasmic sperm injection, in vitro fertilization and natural conception. Hum Reprod 2005; 20 (02) 413-419
  • 19 Davies MJ, Moore VM, Willson KJ. , et al. Reproductive technologies and the risk of birth defects. N Engl J Med 2012; 366 (19) 1803-1813
  • 20 Kissin DM, Zhang Y, Boulet SL. , et al. Association of assisted reproductive technology (ART) treatment and parental infertility diagnosis with autism in ART-conceived children. Hum Reprod 2015; 30 (02) 454-465
  • 21 Ludwig M, Katalinic A. Malformation rate in fetuses and children conceived after ICSI: results of a prospective cohort study. Reprod Biomed Online 2002; 5 (02) 171-178
  • 22 Wen SW, Leader A, White RR. , et al. A comprehensive assessment of outcomes in pregnancies conceived by in vitro fertilization/intracytoplasmic sperm injection. Eur J Obstet Gynecol Reprod Biol 2010; 150 (02) 160-165
  • 23 Ombelet W, Peeraer K, De Sutter P. , et al. Perinatal outcome of ICSI pregnancies compared with a matched group of natural conception pregnancies in Flanders (Belgium): a cohort study. Reprod Biomed Online 2005; 11 (02) 244-253
  • 24 Lambert RD. Safety issues in assisted reproductive technology: aetiology of health problems in singleton ART babies. Hum Reprod 2003; 18 (10) 1987-1991
  • 25 Bonduelle M, Van Assche E, Joris H. , et al. Prenatal testing in ICSI pregnancies: incidence of chromosomal anomalies in 1586 karyotypes and relation to sperm parameters. Hum Reprod 2002; 17 (10) 2600-2614
  • 26 Practice Committees of American Society for Reproductive Medicine; Society for Assisted Reproductive Technology. Mature oocyte cryopreservation: a guideline. Fertil Steril 2013; 99 (01) 37-43
  • 27 Rienzi L, Gracia C, Maggiulli R. , et al. Oocyte, embryo and blastocyst cryopreservation in ART: systematic review and meta-analysis comparing slow-freezing versus vitrification to produce evidence for the development of global guidance. Hum Reprod Update 2017; 23 (02) 139-155
  • 28 Seshadri S, Saab W, Exeter H. , et al. Clinical outcomes of a vitrified donor oocyte programme: a single UK centre experience. Eur J Obstet Gynecol Reprod Biol 2018; 225: 136-140
  • 29 Cobo A, Coello A, Remohí J, Serrano J, de Los Santos JM, Meseguer M. Effect of oocyte vitrification on embryo quality: time-lapse analysis and morphokinetic evaluation. Fertil Steril 2017; 108 (03) 491-497.e3
  • 30 Practice Committees of the American Society for Reproductive Medicine and the Society for Assisted Reproductive Technology. Blastocyst culture and transfer in clinical-assisted reproduction: a committee opinion. Fertil Steril 2013; 99 (03) 667-672
  • 31 Gosden RG. Oogenesis as a foundation for embryogenesis. Mol Cell Endocrinol 2002; 186 (02) 149-153
  • 32 Blake DA, Farquhar CM, Johnson N, Proctor M. Cleavage stage versus blastocyst stage embryo transfer in assisted conception. Cochrane Database Syst Rev 2007; (04) CD002118
  • 33 Glujovsky D, Farquhar C, Quinteiro Retamar AM, Alvarez Sedo CR, Blake D. Cleavage stage versus blastocyst stage embryo transfer in assisted reproductive technology. Cochrane Database Syst Rev 2016; (06) CD002118
  • 34 Zech NH, Lejeune B, Puissant F, Vanderzwalmen S, Zech H, Vanderzwalmen P. Prospective evaluation of the optimal time for selecting a single embryo for transfer: day 3 versus day 5. Fertil Steril 2007; 88 (01) 244-246
  • 35 De Vos A, Van Landuyt L, Santos-Ribeiro S. , et al. Cumulative live birth rates after fresh and vitrified cleavage-stage versus blastocyst-stage embryo transfer in the first treatment cycle. Hum Reprod 2016; 31 (11) 2442-2449
  • 36 Shapiro BS, Richter KS, Harris DC, Daneshmand ST. Influence of patient age on the growth and transfer of blastocyst-stage embryos. Fertil Steril 2002; 77 (04) 700-705
  • 37 Dar S, Librach CL, Gunby J, Bissonnette F, Cowan L. ; IVF Directors Group of Canadian Fertility and Andrology Society. Increased risk of preterm birth in singleton pregnancies after blastocyst versus Day 3 embryo transfer: Canadian ART Register (CARTR) analysis. Hum Reprod 2013; 28 (04) 924-928
  • 38 Kalra SK, Ratcliffe SJ, Barnhart KT, Coutifaris C. Extended embryo culture and an increased risk of preterm delivery. Obstet Gynecol 2012; 120 (01) 69-75
  • 39 Dar S, Lazer T, Shah PS, Librach CL. Neonatal outcomes among singleton births after blastocyst versus cleavage stage embryo transfer: a systematic review and meta-analysis. Hum Reprod Update 2014; 20 (03) 439-448
  • 40 Ginström Ernstad E, Bergh C, Khatibi A. , et al. Neonatal and maternal outcome after blastocyst transfer: a population-based registry study. Am J Obstet Gynecol 2016; 214 (03) 378.e1-378.e10
  • 41 Kleijkers SH, van Montfoort AP, Smits LJ. , et al. IVF culture medium affects post-natal weight in humans during the first 2 years of life. Hum Reprod 2014; 29 (04) 661-669
  • 42 Rizos D, Lonergan P, Boland MP. , et al. Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality. Biol Reprod 2002; 66 (03) 589-595
  • 43 Buck Louis GM, Bell E, Xie Y, Sundaram R, Yeung E. Parental health status and infant outcomes: Upstate KIDS Study. Fertil Steril 2018; 109 (02) 315-323
  • 44 Roustaei Z, Vehviläinen-Julkunen K, Tuomainen TP, Lamminpää R, Heinonen S. The effect of advanced maternal age on maternal and neonatal outcomes of placenta previa: a register-based cohort study. Eur J Obstet Gynecol Reprod Biol 2018; 227: 1-7
  • 45 Leader J, Bajwa A, Lanes A. , et al. The effect of very advanced maternal age on maternal and neonatal outcomes: a systematic review. J Obstet Gynaecol Can 2018; 40 (09) 1208-1218
  • 46 Johnson JA, Tough S. ; SOGC GENETICS COMMITTEE. Delayed child-bearing. J Obstet Gynaecol Can 2012; 34 (01) 80-93
  • 47 Fall CH, Sachdev HS, Osmond C. , et al; COHORTS investigators. Association between maternal age at childbirth and child and adult outcomes in the offspring: a prospective study in five low-income and middle-income countries (COHORTS collaboration). Lancet Glob Health 2015; 3 (07) e366-e377
  • 48 Imterat M, Wainstock T, Sheiner E, Kapelushnik J, Fischer L, Walfisch A. Advanced maternal age during pregnancy and the risk for malignant morbidity in the childhood. Eur J Pediatr 2018; 177 (06) 879-886
  • 49 Yip BH, Pawitan Y, Czene K. Parental age and risk of childhood cancers: a population-based cohort study from Sweden. Int J Epidemiol 2006; 35 (06) 1495-1503
  • 50 Luke B, Brown MB, Wantman E. , et al. Cumulative birth rates with linked assisted reproductive technology cycles. N Engl J Med 2012; 366 (26) 2483-2491
  • 51 Petridou ET, Georgakis MK, Erdmann F. , et al. Advanced parental age as risk factor for childhood acute lymphoblastic leukemia: results from studies of the Childhood Leukemia International Consortium. Eur J Epidemiol 2018; DOI: 10.1007/s10654-018-0402.
  • 52 Oldereid NB, Wennerholm UB, Pinborg A. , et al. The effect of paternal factors on perinatal and paediatric outcomes: a systematic review and meta-analysis. Hum Reprod Update 2018; 24 (03) 320-389
  • 53 Sandin S, Schendel D, Magnusson P. , et al. Autism risk associated with parental age and with increasing difference in age between the parents. Mol Psychiatry 2016; 21 (05) 693-700
  • 54 Yeung EH, Sundaram R, Ghassabian A, Xie Y, Buck Louis G. Parental obesity and early childhood development. Pediatrics 2017; 139 (02) e20161459
  • 55 Surén P, Gunnes N, Roth C. , et al. Parental obesity and risk of autism spectrum disorder. Pediatrics 2014; 133 (05) e1128-e1138
  • 56 Chen Q, Yan W, Duan E. Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications. Nat Rev Genet 2016; 17 (12) 733-743
  • 57 Schagdarsurengin U, Steger K. Epigenetics in male reproduction: effect of paternal diet on sperm quality and offspring health. Nat Rev Urol 2016; 13 (10) 584-595
  • 58 Grandjean V, Fourré S, De Abreu DA, Derieppe MA, Remy JJ, Rassoulzadegan M. RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci Rep 2015; 5: 18193
  • 59 Sanchez CE, Barry C, Sabhlok A. , et al. Maternal pre-pregnancy obesity and child neurodevelopmental outcomes: a meta-analysis. Obes Rev 2018; 19 (04) 464-484
  • 60 Johnson JA, Grande JP, Roche PC, Kumar R. Immunohistochemical detection and distribution of the 1,25-dihydroxyvitamin D3 receptor in rat reproductive tissues. Histochem Cell Biol 1996; 105 (01) 7-15
  • 61 Halloran BP, DeLuca HF. Effect of vitamin D deficiency on fertility and reproductive capacity in the female rat. J Nutr 1980; 110 (08) 1573-1580
  • 62 Pacis MM, Fortin CN, Zarek SM, Mumford SL, Segars JH. Vitamin D and assisted reproduction: should vitamin D be routinely screened and repleted prior to ART? A systematic review. J Assist Reprod Genet 2015; 32 (03) 323-335
  • 63 Hanieh S, Ha TT, Simpson JA. , et al. Maternal vitamin D status and infant outcomes in rural Vietnam: a prospective cohort study. PLoS One 2014; 9 (06) e99005
  • 64 Zhu P, Tong SL, Hao JH. , et al. Cord blood vitamin D and neurocognitive development are nonlinearly related in toddlers. J Nutr 2015; 145 (06) 1232-1238
  • 65 Morales E, Guxens M, Llop S. , et al; INMA Project. Circulating 25-hydroxyvitamin D3 in pregnancy and infant neuropsychological development. Pediatrics 2012; 130 (04) e913-e920
  • 66 Chi MZ, Zhu L, Zhang ZL. , et al. The relationship between maternal serum vitamin D levels and infant neurodevelopment and anthropometry: a prospective observational study. J Nutr Sci Vitaminol (Tokyo) 2018; 64 (02) 161-167
  • 67 Tylavsky FA, Kocak M, Murphy LE. , et al. Gestational vitamin 25(OH)D status as a risk factor for receptive language development: a 24-month, longitudinal, observational study. Nutrients 2015; 7 (12) 9918-9930
  • 68 Darling AL, Rayman MP, Steer CD, Golding J, Lanham-New SA, Bath SC. Association between maternal vitamin D status in pregnancy and neurodevelopmental outcomes in childhood: results from the Avon Longitudinal Study of Parents and Children (ALSPAC). Br J Nutr 2017; 117 (12) 1682-1692
  • 69 Keim SA, Bodnar LM, Klebanoff MA. Maternal and cord blood 25(OH)-vitamin D concentrations in relation to child development and behaviour. Paediatr Perinat Epidemiol 2014; 28 (05) 434-444
  • 70 Daraki V, Roumeliotaki T, Koutra K. , et al. High maternal vitamin D levels in early pregnancy may protect against behavioral difficulties at preschool age: the Rhea mother-child cohort, Crete, Greece. Eur Child Adolesc Psychiatry 2018; 27 (01) 79-88
  • 71 Mossin MH, Aaby JB, Dalgård C, Lykkedegn S, Christesen HT, Bilenberg N. Inverse associations between cord vitamin D and attention deficit hyperactivity disorder symptoms: a child cohort study. Aust N Z J Psychiatry 2017; 51 (07) 703-710
  • 72 Morales E, Julvez J, Torrent M. , et al. Vitamin D in pregnancy and attention deficit hyperactivity disorder-like symptoms in childhood. Epidemiology 2015; 26 (04) 458-465
  • 73 Chen J, Xin K, Wei J, Zhang K, Xiao H. Lower maternal serum 25(OH) D in first trimester associated with higher autism risk in Chinese offspring. J Psychosom Res 2016; 89: 98-101
  • 74 Wu DM, Wen X, Han XR. , et al. Relationship between neonatal vitamin D at birth and risk of autism spectrum disorders: the NBSIB study. J Bone Miner Res 2018; 33 (03) 458-466
  • 75 Fernell E, Bejerot S, Westerlund J. , et al. Autism spectrum disorder and low vitamin D at birth: a sibling control study. Mol Autism 2015; 6 (03) 3
  • 76 Gustafsson P, Rylander L, Lindh CH. , et al. Vitamin D status at birth and future risk of attention deficit/hyperactivity disorder (ADHD). PLoS One 2015; 10 (10) e0140164
  • 77 Strøm M, Halldorsson TI, Hansen S. , et al. Vitamin D measured in maternal serum and offspring neurodevelopmental outcomes: a prospective study with long-term follow-up. Ann Nutr Metab 2014; 64 (3-4): 254-261
  • 78 Whitehouse AJ, Holt BJ, Serralha M, Holt PG, Kusel MM, Hart PH. Maternal serum vitamin D levels during pregnancy and offspring neurocognitive development. Pediatrics 2012; 129 (03) 485-493
  • 79 Veena SR, Krishnaveni GV, Srinivasan K. , et al. Association between maternal vitamin D status during pregnancy and offspring cognitive function during childhood and adolescence. Asia Pac J Clin Nutr 2017; 26 (03) 438-449
  • 80 Gale CR, Robinson SM, Harvey NC. , et al; Princess Anne Hospital Study Group. Maternal vitamin D status during pregnancy and child outcomes. Eur J Clin Nutr 2008; 62 (01) 68-77
  • 81 Laird E, Thurston SW, van Wijngaarden E. , et al. Maternal vitamin D status and the relationship with neonatal anthropometric and childhood neurodevelopmental outcomes: results from the Seychelles Child Development Nutrition Study. Nutrients 2017; 9 (11) E1235
  • 82 Dumesic DA, Oberfield SE, Stener-Victorin E, Marshall JC, Laven JS, Legro RS. Scientific statement on the diagnostic criteria, epidemiology, pathophysiology, and molecular genetics of polycystic ovary syndrome. Endocr Rev 2015; 36 (05) 487-525
  • 83 Lauritsen MP, Bentzen JG, Pinborg A. , et al. The prevalence of polycystic ovary syndrome in a normal population according to the Rotterdam criteria versus revised criteria including anti-Mullerian hormone. Hum Reprod 2014; 29 (04) 791-801
  • 84 March WA, Moore VM, Willson KJ, Phillips DI, Norman RJ, Davies MJ. The prevalence of polycystic ovary syndrome in a community sample assessed under contrasting diagnostic criteria. Hum Reprod 2010; 25 (02) 544-551
  • 85 Kuijper EA, Vink JM, Lambalk CB, Boomsma DI. Prevalence of polycystic ovary syndrome in women from opposite-sex twin pairs. J Clin Endocrinol Metab 2009; 94 (06) 1987-1990
  • 86 Vink JM, Sadrzadeh S, Lambalk CB, Boomsma DI. Heritability of polycystic ovary syndrome in a Dutch twin-family study. J Clin Endocrinol Metab 2006; 91 (06) 2100-2104
  • 87 Boomsma CM, Eijkemans MJ, Hughes EG, Visser GH, Fauser BC, Macklon NS. A meta-analysis of pregnancy outcomes in women with polycystic ovary syndrome. Hum Reprod Update 2006; 12 (06) 673-683
  • 88 Doherty DA, Newnham JP, Bower C, Hart R. Implications of polycystic ovary syndrome for pregnancy and for the health of offspring. Obstet Gynecol 2015; 125 (06) 1397-1406
  • 89 Bell GA, Sundaram R, Mumford SL. , et al. Maternal polycystic ovarian syndrome and early offspring development. Hum Reprod 2018; 33 (07) 1307-1315
  • 90 Kosidou K, Dalman C, Widman L. , et al. Maternal polycystic ovary syndrome and the risk of autism spectrum disorders in the offspring: a population-based nationwide study in Sweden. Mol Psychiatry 2016; 21 (10) 1441-1448
  • 91 Kosidou K, Dalman C, Widman L. , et al. Maternal polycystic ovary syndrome and risk for attention-deficit/hyperactivity disorder in the offspring. Biol Psychiatry 2017; 82 (09) 651-659
  • 92 Berni TR, Morgan CL, Berni ER, Rees DA. Polycystic ovary syndrome is associated with adverse mental health and neurodevelopmental outcomes. J Clin Endocrinol Metab 2018; 103 (06) 2116-2125
  • 93 Palomba S, Marotta R, Di Cello A. , et al. Pervasive developmental disorders in children of hyperandrogenic women with polycystic ovary syndrome: a longitudinal case-control study. Clin Endocrinol (Oxf) 2012; 77 (06) 898-904
  • 94 Bell GA, Sundaram R, Mumford SL. , et al. Maternal polycystic ovarian syndrome and offspring growth: the Upstate KIDS Study. J Epidemiol Community Health 2018; 72 (09) 852-855
  • 95 Auyeung B, Baron-Cohen S, Ashwin E, Knickmeyer R, Taylor K, Hackett G. Fetal testosterone and autistic traits. Br J Psychol 2009; 100 (Pt 1): 1-22
  • 96 Auyeung B, Taylor K, Hackett G, Baron-Cohen S. Foetal testosterone and autistic traits in 18 to 24-month-old children. Mol Autism 2010; 1 (01) 11
  • 97 Hines M. Prenatal endocrine influences on sexual orientation and on sexually differentiated childhood behavior. Front Neuroendocrinol 2011; 32 (02) 170-182
  • 98 Hu M, Richard JE, Maliqueo M. , et al. Maternal testosterone exposure increases anxiety-like behavior and impacts the limbic system in the offspring. Proc Natl Acad Sci U S A 2015; 112 (46) 14348-14353
  • 99 Manson JE. Prenatal exposure to sex steroid hormones and behavioral/cognitive outcomes. Metabolism 2008; 57 (Suppl. 02) S16-S21
  • 100 Puttabyatappa M, Cardoso RC, Padmanabhan V. Effect of maternal PCOS and PCOS-like phenotype on the offspring's health. Mol Cell Endocrinol 2016; 435: 29-39
  • 101 Poppe K, Velkeniers B, Glinoer D. The role of thyroid autoimmunity in fertility and pregnancy. Nat Clin Pract Endocrinol Metab 2008; 4 (07) 394-405
  • 102 Wakim AN, Polizotto SL, Buffo MJ, Marrero MA, Burholt DR. Thyroid hormones in human follicular fluid and thyroid hormone receptors in human granulosa cells. Fertil Steril 1993; 59 (06) 1187-1190
  • 103 Krassas GE. Thyroid disease and female reproduction. Fertil Steril 2000; 74 (06) 1063-1070
  • 104 Orouji Jokar T, Fourman LT, Lee H, Mentzinger K, Fazeli PK. Higher TSH levels within the normal range are associated with unexplained infertility. J Clin Endocrinol Metab 2018; 103 (02) 632-639
  • 105 Poppe K, Velkeniers B. Thyroid disorders in infertile women. Ann Endocrinol (Paris) 2003; 64 (01) 45-50
  • 106 Plowden TC, Schisterman EF, Sjaarda LA. , et al. Subclinical hypothyroidism and thyroid autoimmunity are not associated with fecundity, pregnancy loss, or live birth. J Clin Endocrinol Metab 2016; 101 (06) 2358-2365
  • 107 Brabant G, Beck-Peccoz P, Jarzab B. , et al. Is there a need to redefine the upper normal limit of TSH?. Eur J Endocrinol 2006; 154 (05) 633-637
  • 108 Lavado-Autric R, Ausó E, García-Velasco JV. , et al. Early maternal hypothyroxinemia alters histogenesis and cerebral cortex cytoarchitecture of the progeny. J Clin Invest 2003; 111 (07) 1073-1082
  • 109 Cuevas E, Ausó E, Telefont M, Morreale de Escobar G, Sotelo C, Berbel P. Transient maternal hypothyroxinemia at onset of corticogenesis alters tangential migration of medial ganglionic eminence-derived neurons. Eur J Neurosci 2005; 22 (03) 541-551
  • 110 Bernal J. Thyroid hormones and brain development. Vitam Horm 2005; 71: 95-122
  • 111 Kester MHA, Martinez de Mena R, Obregon MJ. , et al. Iodothyronine levels in the human developing brain: major regulatory roles of iodothyronine deiodinases in different areas. J Clin Endocrinol Metab 2004; 89 (07) 3117-3128
  • 112 Morreale de Escobar G, Obregon MJ, Escobar del Rey F. Role of thyroid hormone during early brain development. Eur J Endocrinol 2004; 151 (Suppl. 03) U25-U37
  • 113 Korevaar TIM, Medici M, Visser TJ, Peeters RP. Thyroid disease in pregnancy: new insights in diagnosis and clinical management. Nat Rev Endocrinol 2017; 13 (10) 610-622
  • 114 Haddow JE, Palomaki GE, Allan WC. , et al. Maternal thyroid deficiency during pregnancy and subsequent neuropsychological development of the child. N Engl J Med 1999; 341 (08) 549-555
  • 115 Lischinsky JE, Skocic J, Clairman H, Rovet J. Preliminary findings show maternal hypothyroidism may contribute to abnormal cortical morphology in offspring. Front Endocrinol (Lausanne) 2016; 7: 16
  • 116 Samadi A, Skocic J, Rovet JF. Children born to women treated for hypothyroidism during pregnancy show abnormal corpus callosum development. Thyroid 2015; 25 (05) 494-502
  • 117 Alexander EK, Pearce EN, Brent GA. , et al. 2017 Guidelines of the American Thyroid Association for the diagnosis and management of thyroid disease during pregnancy and the postpartum. Thyroid 2017; 27 (03) 315-389
  • 118 De Groot L, Abalovich M, Alexander EK. , et al. Management of thyroid dysfunction during pregnancy and postpartum: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 2012; 97 (08) 2543-2565
  • 119 Smit BJ, Kok JH, Vulsma T, Briët JM, Boer K, Wiersinga WM. Neurologic development of the newborn and young child in relation to maternal thyroid function. Acta Paediatr 2000; 89 (03) 291-295
  • 120 Li Y, Shan Z, Teng W. , et al. Abnormalities of maternal thyroid function during pregnancy affect neuropsychological development of their children at 25-30 months. Clin Endocrinol (Oxf) 2010; 72 (06) 825-829
  • 121 Ghassabian A, El Marroun H, Peeters RP. , et al. Downstream effects of maternal hypothyroxinemia in early pregnancy: nonverbal IQ and brain morphology in school-age children. J Clin Endocrinol Metab 2014; 99 (07) 2383-2390
  • 122 Henrichs J, Bongers-Schokking JJ, Schenk JJ. , et al. Maternal thyroid function during early pregnancy and cognitive functioning in early childhood: the generation R study. J Clin Endocrinol Metab 2010; 95 (09) 4227-4234
  • 123 Ghassabian A, Bongers-Schokking JJ, Henrichs J. , et al. Maternal thyroid function during pregnancy and behavioral problems in the offspring: the generation R study. Pediatr Res 2011; 69 (5, Pt 1): 454-459
  • 124 Andersen SL, Andersen S, Liew Z, Vestergaard P, Olsen J. Maternal thyroid function in early pregnancy and neuropsychological performance of the child at 5 years of age. J Clin Endocrinol Metab 2018; 103 (02) 660-670
  • 125 Modesto T, Tiemeier H, Peeters RP. , et al. Maternal mild thyroid hormone insufficiency in early pregnancy and attention-deficit/hyperactivity disorder symptoms in children. JAMA Pediatr 2015; 169 (09) 838-845
  • 126 Oostenbroek MHW, Kersten RHJ, Tros B, Kunst AE, Vrijkotte TGM, Finken MJJ. Maternal hypothyroxinaemia in early pregnancy and problem behavior in 5-year-old offspring. Psychoneuroendocrinology 2017; 81: 29-35
  • 127 Román GC, Ghassabian A, Bongers-Schokking JJ. , et al. Association of gestational maternal hypothyroxinemia and increased autism risk. Ann Neurol 2013; 74 (05) 733-742
  • 128 Levie D, Korevaar TIM, Bath SC. , et al. Thyroid function in early pregnancy, child IQ, and autistic traits: a meta-analysis of individual participant data. J Clin Endocrinol Metab 2018; 103 (08) 2967-2979
  • 129 Gyllenberg D, Sourander A, Surcel HM, Hinkka-Yli-Salomäki S, McKeague IW, Brown AS. Hypothyroxinemia during gestation and offspring schizophrenia in a national birth cohort. Biol Psychiatry 2016; 79 (12) 962-970
  • 130 Korevaar TIM, Muetzel R, Medici M. , et al. Association of maternal thyroid function during early pregnancy with offspring IQ and brain morphology in childhood: a population-based prospective cohort study. Lancet Diabetes Endocrinol 2016; 4 (01) 35-43
  • 131 Päkkilä F, Männistö T, Hartikainen A-L, Suvanto E. maternal thyroid function during pregnancy and the child's linguistic and sensory development in the Northern Finland Birth Cohort 1986. Front Endocrinol (Lausanne) 2018; 9: 127
  • 132 Lazarus JH, Bestwick JP, Channon S. , et al. Antenatal thyroid screening and childhood cognitive function. N Engl J Med 2012; 366 (06) 493-501
  • 133 Casey BM, Thom EA, Peaceman AM. , et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Maternal–Fetal Medicine Units Network. Treatment of subclinical hypothyroidism or hypothyroxinemia in pregnancy. N Engl J Med 2017; 376 (09) 815-825
  • 134 Brent GA. The debate over thyroid-function screening in pregnancy. N Engl J Med 2012; 366 (06) 562-563
  • 135 Korevaar TIM, Chaker L, Peeters RP. Improving the clinical impact of randomised trials in thyroidology. Lancet Diabetes Endocrinol 2018; 6 (07) 523-525
  • 136 Fassino S, Abbate-Daga G, Amianto F, Leombruni P, Boggio S, Rovera GG. Temperament and character profile of eating disorders: a controlled study with the Temperament and Character Inventory. Int J Eat Disord 2002; 32 (04) 412-425
  • 137 Lakatos E, Szigeti JF, Ujma PP, Sexty R, Balog P. Anxiety and depression among infertile women: a cross-sectional survey from Hungary. BMC Womens Health 2017; 17 (01) 48
  • 138 Drosdzol A, Skrzypulec V. Depression and anxiety among Polish infertile couples--an evaluative prevalence study. J Psychosom Obstet Gynaecol 2009; 30 (01) 11-20
  • 139 Yang B, Zhang J, Qi Y, Wang P, Jiang R, Li H. Assessment on occurrences of depression and anxiety and associated risk factors in the infertile Chinese men. Am J Men Health 2017; 11 (03) 767-774
  • 140 Greil AL. Infertility and psychological distress: a critical review of the literature. Soc Sci Med 1997; 45 (11) 1679-1704
  • 141 Bhongade MB, Prasad S, Jiloha RC, Ray PC, Mohapatra S, Koner BC. Effect of psychological stress on fertility hormones and seminal quality in male partners of infertile couples. Andrologia 2015; 47 (03) 336-342
  • 142 Guxens M, Tiemeier H, Jansen PW. , et al. Parental psychological distress during pregnancy and early growth in preschool children: the generation R study. Am J Epidemiol 2013; 177 (06) 538-547
  • 143 Lampard AM, Franckle RL, Davison KK. Maternal depression and childhood obesity: a systematic review. Prev Med 2014; 59: 60-67
  • 144 Jarde A, Morais M, Kingston D. , et al. Neonatal outcomes in women with untreated antenatal depression compared with women without depression: a systematic review and meta-analysis. JAMA Psychiatry 2016; 73 (08) 826-837
  • 145 Kingston D, Kehler H, Austin MP. , et al. Trajectories of maternal depressive symptoms during pregnancy and the first 12 months postpartum and child externalizing and internalizing behavior at three years. PLoS One 2018; 13 (04) e0195365
  • 146 Vafai Y, Steinberg JR, Shenassa ED. Maternal postpartum depressive symptoms and infant externalizing and internalizing behaviors. Infant Behav Dev 2016; 42: 119-127
  • 147 Park H, Sundaram R, Gilman SE, Bell G, Louis GMB, Yeung EH. Timing of maternal depression and sex-specific child growth, the Upstate KIDS Study. Obesity (Silver Spring) 2018; 26 (01) 160-166
  • 148 van der Waerden J, Bernard JY, De Agostini M. , et al; EDEN Mother-Child Cohort Study Group. Persistent maternal depressive symptoms trajectories influence children's IQ: The EDEN mother-child cohort. Depress Anxiety 2017; 34 (02) 105-117
  • 149 Kim P, Swain JE. Sad dads: paternal postpartum depression. Psychiatry (Edgmont Pa) 2007; 4 (02) 35-47
  • 150 O'Brien AP, McNeil KA, Fletcher R. , et al. New fathers' perinatal depression and anxiety-treatment options: an integrative review. Am J Men Health 2017; 11 (04) 863-876
  • 151 Paulson JF, Bazemore SD. Prenatal and postpartum depression in fathers and its association with maternal depression: a meta-analysis. JAMA 2010; 303 (19) 1961-1969
  • 152 Takehara K, Suto M, Kakee N, Tachibana Y, Mori R. Prenatal and early postnatal depression and child maltreatment among Japanese fathers. Child Abuse Negl 2017; 70: 231-239
  • 153 Ramchandani P, Stein A, Evans J, O'Connor TG. ; ALSPAC study team. Paternal depression in the postnatal period and child development: a prospective population study. Lancet 2005; 365 (9478): 2201-2205
  • 154 Gutierrez-Galve L, Stein A, Hanington L, Heron J, Ramchandani P. Paternal depression in the postnatal period and child development: mediators and moderators. Pediatrics 2015; 135 (02) e339-e347
  • 155 Cameron EE, Sedov ID, Tomfohr-Madsen LM. Prevalence of paternal depression in pregnancy and the postpartum: an updated meta-analysis. J Affect Disord 2016; 206: 189-203
  • 156 Fadhlaoui A, Bouquet de la Jolinière J, Feki A. Endometriosis and infertility: how and when to treat?. Front Surg 2014; 1: 24
  • 157 Mu F, Harris HR, Rich-Edwards JW. , et al. A prospective study of inflammatory markers and risk of endometriosis. Am J Epidemiol 2018; 187 (03) 515-522
  • 158 Mu F, Rich-Edwards J, Rimm EB, Spiegelman D, Forman JP, Missmer SA. Association between endometriosis and hypercholesterolemia or hypertension. Hypertension 2017; 70 (01) 59-65
  • 159 Mu F, Rich-Edwards J, Rimm EB, Spiegelman D, Missmer SA. Endometriosis and risk of coronary heart disease. Circ Cardiovasc Qual Outcomes 2016; 9 (03) 257-264
  • 160 Stewart EA, Cookson CL, Gandolfo RA, Schulze-Rath R. Epidemiology of uterine fibroids: a systematic review. BJOG 2017; 124 (10) 1501-1512
  • 161 Uimari O, Auvinen J, Jokelainen J. , et al. Uterine fibroids and cardiovascular risk. Hum Reprod 2016; 31 (12) 2689-2703
  • 162 Greenland S, Pearl J, Robins JM. Causal diagrams for epidemiologic research. Epidemiology 1999; 10 (01) 37-48
  • 163 Fox MP, Lash TL. On the need for quantitative bias analysis in the peer-review process. Am J Epidemiol 2017; 185 (10) 865-868
  • 164 von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. ; STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: guidelines for reporting observational studies. Int J Surg 2014; 12 (12) 1495-1499