A systematic review and meta-analysis of DNA methylation levels and imprinting disorders in children conceived by IVF/ICSI compared with children conceived spontaneously

Human Reproduction Update

Volumn 20, Issue 6, 2014, Pages 840-852

  Lazaraviciute, Gabija ^a   Kauser, Miriam ^a   Bhattacharya, Sohinee ^a   Haggarty, Paul ^b   Bhattacharya, Siladitya ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b ROWETT RESEARCH INSTITUTE   (United Kingdom)

Author keywords

DNA methylation; Epigenetic disorders; ICSI; Imprinting disorders; IVF

Indexed keywords

DNA; GROWTH FACTOR RECEPTOR BOUND PROTEIN 10; H19 LONG NON-CODING RNA; KCNQ1OT1 PROTEIN, HUMAN; LONG UNTRANSLATED RNA; MESODERM SPECIFIC TRANSCRIPT PROTEIN; PROTEIN; SMALL NUCLEAR RIBONUCLEOPROTEIN; VOLTAGE GATED POTASSIUM CHANNEL;

ARTICLE; CASE CONTROL STUDY; CHILD; CHILDHOOD DISEASE; COHORT ANALYSIS; COMPARATIVE STUDY; DNA METHYLATION; EPIGENETICS; FERTILITY; FERTILIZATION IN VITRO; GENE; GENETIC DISORDER; GRB10 GENE; HI9 GENE; HUMAN; IGF2 GENE; INFERTILITY; INTRACYTOPLASMIC SPERM INJECTION; KCNQ10T1 GENE; KVDMR GENE; MEST GENE; OBSERVATIONAL STUDY; OUTCOME ASSESSMENT; PEG3 GENE; PEGI GENE; SNRPN GENE; SYSTEMATIC REVIEW; ADVERSE EFFECTS; GENOME IMPRINTING; META ANALYSIS; PHYSIOLOGY;

CHILD; COHORT STUDIES; DNA METHYLATION; FERTILIZATION IN VITRO; GENOMIC IMPRINTING; GRB10 ADAPTOR PROTEIN; HUMANS; INFERTILITY; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEINS; RNA, LONG NONCODING; SNRNP CORE PROTEINS; SPERM INJECTIONS, INTRACYTOPLASMIC;

EID: 84913603626     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmu033     Document Type: Article

References (57)

1. Batcheller A, Cardozo E, Maguire M, DeCherney AH, Segars JH. Are there subtle genome-wide epigenetic alterations in normal offspring conceived by assisted reproductive technologies? Fertil Steril 2011;96:1306-1311.
2. Byun H-M, Siegmund KD, Pan F, Weisenberger DJ, Kanel G, Laird PW, Yang AS. Epigenetic profiling of somatic tissues from human autopsy specimens identifies tissue- and individual-specific DNA methylation patterns. Hum Mol Genet 2009; 18:4808-4817.
3. Cedars MI. In vitro fertilization and risk of autistic disorder and mental retardation. JAMA 2013;310:42-43.
4. Ceelen M, Van Weissenbruch MM, Roos JC, Vermeiden JPW, Van Leeuwen FE, Delemarre-van DeWaal HA. Body composition in children and adolescents born after in vitro fertilization or spontaneous conception. J Clin Endocrinol Metab 2007; 92:3417-3423.
5. Ceelen M, VanWeissenbruch MM, Vermeiden JPW, Van Leeuwen FE, Delemarre-Van DeWaal HA. Cardiometabolic differences in children born after in vitro fertilization: follow-up study. J Clin Endocrinol Metab 2008;93:1682-1688.
6. ChanWong E, Hatakeyama C, Robinson WP, Ma S. DNA methylation at H19/IGF2 ICR1 in the placenta of pregnancies conceived by in vitro fertilization and intracytoplasmic sperm injection. Fertil Steril 2011a;95:2524-2526.e3.
7. ChanWong E, Hatakeyama C, Robinson WP, Ma S. DNA methylation at H19/IGF2 ICR1 in the placenta of pregnancies conceived by IVF and ICSI. Human Reproduction. Conference: 27th Annual Meeting of the European Society of Human Reproduction and Embryology, ESHRE 2011 Stockholm Sweden. Conference Start: 20110703 Conference End: 20110706. Conference Publication: (var.pagings) 2011b; 26:77.
8. Coolen MW, Statham AL, Qu W, Campbell MJ, Henders AK, Montgomery GW, Martin NG, Clark SJ. Impact of the genome on the epigenome is manifested in DNA methylation patterns of imprinted regions in monozygotic and dizygotic twins. PLoS One 2011;6:1-12.e25590.
9. Davies MJ, Moore VM, Willson KJ, Van Essen P, Priest K, Scott H, Haan EA, Chan A. Reproductive technologies and the risk of birth defects. Obstet Gynecol Surv 2012; 67:527-528.
10. Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health 1998;52:377-384.
11. Edwards RG. Aspects of the molecular regulation of early mammalian development. Reprod Biomed Online 2003;6:97-113.
12. Feng C, Tian S, Zhang Y, He J, Zhu X-M, Zhang D, Sheng J-Z, Huang H-F. General imprinting status is stable in assisted reproduction-conceived offspring. Fertil Steril 2011;96:1417-1423.e9.
13. Ferguson-Smith AC, Patti M-E. You are what your dad ate. Cell Metab 2011; 13:115-117.
14. Ferguson-Smith AC, Moore T, Detmar J, Lewis A, Hemberger M, Jammes H, Kelsey G, RobertsCT, Jones H, Constancia M. Epigenetics and imprinting of the trophoblast- a workshop report. Placenta 2006;27:122-126.
15. Fukuda Y, Katagiri Y, Monta M. Investigation of imprinted gene expression for in vitro fertilized mouse embryos. J Mamm Ova Res 2010;27:51-57.
16. Gomes MV, Huber J, Ferriani RA, Amaral Neto AM, Ramos ES. Abnormal methylation at the KvDMR1 imprinting control region in clinically normal children conceived by assisted reproductive technologies. Mol Hum Reprod 2009;15:471-477.
17. Gosden R, Trasler J, Lucifero D, Faddy M. Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet 2003;361:1975-1977.
18. Guo L, Choufani S, Ferreira J, Smith A, Chitayat D, Shuman C, Uxa R, Keating S, Kingdom J, Weksberg R. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev Biol 2008;320:79-91.
19. Hackett JA, Surani MA. DNA methylation dynamics during the mammalian life cycle. Philos Trans R Soc Lond B Biol Sci 2013;368:20110328.
20. Haggarty P, Ferguson-Smith AC. Life course epigenetics and healthy ageing. In: Kuh D, Cooper R, Hardy R, Richards M, Ben-Shlomo I (eds). A Life Course Approach to Healthy Ageing. UK: Oxford University Press, 2013, 198-212.
21. Halliday J, Oke K, Breheny S, Algar E, Amor DJ. Beckwith-Wiedemann syndrome and IVF: a case-control study [4]. Am J Hum Genet 2004;75:526-528.
22. Hammoud SS, Purwar J, Pflueger C, Cairns BR, Carrell DT. Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility. Fertil Steril 2010; 94:1728-1733.
23. Hansen M, Kurinczuk JJ, Bower C,Webb S, Bergh C. Children conceived by IVF or ICSI were twice as likely as naturally conceived children to have major birth defects. Evid Based Obstet Gynecol 2002;4:191-192.
24. Hansen M, Kurinczuk JJ, De Klerk N, Burton P, Bower C. Assisted reproductive technology and major birth defects in Western Australia. Obstet Gynecol 2012; 120:852-863.
25. Hansen M, Kurinczuk JJ, Milne E, de Klerk N, Bower C. Assisted reproductive technology and birth defects: A systematic review and meta-analysis. Hum Reprod Update 2013;19:330-353.
26. Hiura H, Okae H, Miyauchi N, Sato F, Sato A, Van De Pette M, John RM, Kagami M, Nakai K, Soejima H et al. Characterization of DNA methylation errors in patients with imprinting disorders conceived by assisted reproduction technologies. Hum Reprod 2012;27:2541-2548.
27. Kamphuis EI, Bhattacharya S, van der Veen F, Mol BWJ, Templeton A, the Evidence Based IVF Group. Are we overusing IVF? BMJ 2014;348:g252.
28. Kanaka-Gantenbein C, Sakka S, Chrousos GP. Assisted reproduction and its neuroendocrine impact on the offspring. Prog Brain Res 2010;182:161-174.
29. Kanber D, Buiting K, Zeschnigk M, Ludwig M, Horsthemke B. Low frequency of imprinting defects in ICSI children born small for gestational age. Eur J Hum Genet 2009;17:22-29.
30. Katari S, Turan N, Bibikova M, Erinle O, Chalian R, Foster M, Gaughan JP, Coutifaris C, Sapienza C.DNAmethylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet 2009;18:3769-3778.
31. King JL, Yang B, Sparks AET, Mains LM, Murray JC, Van Voorhis BJ. Skewed X inactivation and IVF-conceived infants. Reprod Biomed Online 2010;20:660-663.
32. Le Bouc Y, Rossignol S, Azzi S, Steunou V, Netchine I, Gicquel C. Epigenetics, genomic imprinting and assisted reproductive technology. Ann Endocrinol 2010;71:237-238.
33. Li L,Wang L, Le F, Liu X, Yu P, Sheng J, Huang H, Jin F. Evaluation of DNA methylation status at differentially methylated regions in IVF-conceived newborn twins. Fertil Steril 2011;95:1975-1979.
34. Lidegaard O, Pinborg A, Andersen AN. Imprinting diseases and IVF: Danish National IVF cohort study. Hum Reprod 2005;20:950-954.
35. Manipalviratn S, DeCherney A, Segars J. Imprinting disorders and assisted reproductive technology. Fertil Steril 2009;91:305-315.
36. Melamed N, Choufani S, Wilkins-Haug L, Greenblatt E,Weksberg R. Comparison of genome-wide and gene-specific DNA methylation between pregnancies conceived naturally versus ART (assisted reproductive technologies). Placenta 2013;34:A56.
37. Nelissen ECM, Dumoulin JCM, Daunay A, Evers JLH, Tost J, Van Montfoort APA. Placentas from pregnancies conceived by IVF/ICSI have a reduced DNA methylation level at the H19 and MEST differentially methylated regions. Hum Reprod 2013;28:1117-1126.
38. Odom LN, Segars J. Imprinting disorders and assisted reproductive technology. Curr Opin Endocrinol Diabetes Obes 2010;17:517-522.
39. Oliver VF, Miles HL, Cutfield WS, Hofman PL, Ludgate JL, Morison IM. Defects in imprinting and genome-wide DNA methylation are not common in the in vitro fertilization population. Fertil Steril 2012;97:147-153.e7.
40. Owen CM, Segars Jr JH. Imprinting disorders and assisted reproductive technology. Semin Reprod Med 2009;27:417-428.
41. Puumala SE, Nelson HH, Ross JA, Nguyen RH, Damario MA, Spector LG. SimilarDNA methylation levels in specific imprinting control regions in children conceived with and without assisted reproductive technology: a cross-sectional study. BMC Pediatr 2012;12:33.
42. Rancourt RC, Harris HR, Michels KB. Methylation levels at imprinting control regions are not altered with ovulation induction or in vitro fertilization in a birth cohort. Hum Reprod 2012;27:2208-2216.
43. Rossignol S, Steunou V, Chalas C, Kerjean A, Rigolet M, Viegas-Pequignot E, Jouannet P, Le Bouc Y, Gicquel C. 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;43:902-907.
44. Sakka SD, Malamitsi-Puchner A, Loutradis D, Chrousos GP, Kanaka-Gantenbein C. Euthyroid hyperthyrotropinemia in children born after in vitro fertilization. J Clin Endocrinol Metab 2009;94:1338-1341.
45. Sakka SD, Loutradis D, Kanaka-Gantenbein C, Margeli A, Papastamataki M, Papassotiriou I, Chrousos GP. Absence of insulin resistance and low-grade inflammation despite early metabolic syndrome manifestations in children born after in vitro fertilization. Fertil Steril 2010;94:1693-1699.
46. Sanchez-Albisua I, Borell-Kost S, Mau-Holzmann UA, Licht P, Krageloh-Mann I. Increased frequency of severe major anomalies in children conceived by intracytoplasmic sperm injection. Dev Med Child Neurol 2007;49:129-134.
47. Sandovici I, Leppert M, Hawk PR, Suarez A, Linares Y, Sapienza C. Familial aggregation of abnormal methylation of parental alleles at the IGF2/H19 and IGF2R differentially methylated regions. Hum Mol Genet 2003;12:1569-1578.
48. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 2008;9:129-140.
49. Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 2007;22:26-35.
50. Tierling S, Souren NY, Gries J, Loporto C, Groth M, Lutsik P, Neitzel H, Utz-Billing I, Gillessen-Kaesbach G, Kentenich H et al. Assisted reproductive technologies do not enhance the variability of DNA methylation imprints in human. J Med Genet 2010;47:371-376.
51. Turan N, Katari S, Gerson LF, Chalian R, Foster MW, Gaughan JP, Coutifaris C, Sapienza C. Inter- and intra-individual variation in allele-specific DNA methylation and gene expression in children conceived using assisted reproductive technology. PLoS Genet 2010;6:e1001033.
52. VermeidenJPW, Bernardus RE. Are imprinting disorders moreprevalent afterhuman in vitro fertilization or intracytoplasmic sperm injection? Fertil Steril 2013;99:642-651.
53. White HE, Durston VJ, Harvey JF, Cross NCP. Quantitative analysis of SRNPN gene methylation by pyrosequencing as a diagnostic test for Prader-Willi syndrome and Angelman syndrome. Clin Chem 2006;52:1005-1013.
54. Wilkins JF, Haig D. What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 2003;4:359-368.
55. Woodfine K, Huddleston JE, Murrell A. Quantitative analysis ofDNAmethylation at all human imprinted regions reveals preservation of epigenetic stability in adult somatic tissue. Epigenetics Chromatin 2011;4:1-13.
56. Zechner U, Pliushch G, Schneider E, Hajj NE, Tresch A, Shufaro Y, Seidmann L, Coerdt W, Müller AM, Haaf T. Quantitative methylation analysis of developmentally important genes in human pregnancy losses after ART and spontaneous conception. Mol Hum Reprod 2009;16:704-713.
57. Zheng H-Y, Tang Y, Niu J, Li P, Ye D-S, Chen X, Shi X-Y, Li L, Chen S-L. Aberrant DNA methylation of imprinted loci in human spontaneous abortions after assisted reproduction techniques and natural conception. Hum Reprod 2013; 28:265-273.