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Comprehensive meta-analysis reveals association between multiple imprinting disorders and conception by assisted reproductive technology

  • Victoria K. CortessisEmail author
  • Moosa Azadian
  • James Buxbaum
  • Fatimata Sanogo
  • Ashley Y. Song
  • Intira Sriprasert
  • Pengxiao C. Wei
  • Jing Yu
  • Karine Chung
  • Kimberly D. Siegmund
Review

Abstract

Purpose

To determine whether a history of conception by assisted reproductive technology (ART) is associated with occurrence of one or more imprinting disorders of either maternal or paternal origin.

Methods

We implemented a systematic review of scholarly literature followed by comprehensive meta-analysis to quantitatively synthesize data from reports relating to use of ART to occurrence of any imprinting disorder of humans, including Beckwith-Wiedemann (BWS), Angelman (AS), Prader-Willi (PWS), and Silver-Russell (SRS) syndromes, as well as transient neonatal diabetes mellitus (TNDB) and sporadic retinoblasoma (RB).

Results

The systematic review identified 13 reports presenting unique data from 23 studies that related conception following ART to occurrence of imprinting disorders. Multiple studies of four disorder were identified, for which meta-analysis yielded the following summary estimates of associations with a history of ART: AS, summary odds ratio (sOR) = 4.7 (95% confidence interval (CI) 2.6–8.5, 4 studies); BWS, sOR = 5.8 (95% CI 3.1–11.1, 8 studies); PWS, sOR = 2.2 (95% CI 1.6–3.0, 6 studies); SRS, sOR = 11.3 (95% CI 4.5–28.5, 3 studies). Only one study reported on each of TNDB and RB.

Conclusion

Published data reveal positive associations between history of ART conception and each of four imprinting disorders. Reasons for these associations warrant further investigation.

Keywords

Assisted reproduction Imprinting disorder Beckwith-Wiedemann syndrome Angelman syndrome Prader-Willi syndrome Silver-Russell syndrome 

Notes

Acknowledgments

The authors gratefully acknowledge expert instruction in systematic search provided by Lynn 1. Kysh, MLIS, and Robert E. Johnson, MLIS. This work was supported in part by grants R56ES017091 and P30 ES07048 from the National Institute of Environmental Health Sciences, and LG-99-17-0069 from the Institute of Museum and Library Sciences.

Supplementary material

10815_2018_1173_MOESM1_ESM.pdf (633 kb)
ESM 1 (PDF 633 kb)

References

  1. 1.
    Cox GF, Burger J, Lip V, et al. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am J Hum Genet. 2002;71:162–4.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Orstavik KH, Eiklid K, van der Hagen CB, et al. Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection. Am J Hum Genet. 2003;72:218–9.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Tesarik J, Sousa M, Greco E, Mendoza C. Spermatids as gametes: indications and limitations. Hum Reprod. 1998;13(Suppl 3):89–107. discussion 8-11CrossRefPubMedGoogle Scholar
  4. 4.
    Manning M, Lissens W, Bonduelle M, Camus M, de Rijcke M, Liebaers I, et al. Study of DNA-methylation patterns at chromosome 15q11-q13 in children born after ICSI reveals no imprinting defects. Mol Hum Reprod. 2000;6:1049–53.Google Scholar
  5. 5.
    Young LE, Fernandes K, McEvoy TG, et al. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat Genet. 2001;27:153–4.Google Scholar
  6. 6.
    Surani MA, Barton SC, Norris ML. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature. 1984;308:548–50.CrossRefPubMedGoogle Scholar
  7. 7.
    Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet. 2001;2:21–32.CrossRefPubMedGoogle Scholar
  8. 8.
    Buitendijk SE. Children after in vitro fertilization. An overview of the literature. Int J Technol Assess Health Care. 1999;15:52–65.CrossRefPubMedGoogle Scholar
  9. 9.
    Schieve LA, Meikle SF, Ferre C, Peterson HB, Jeng G, Wilcox LS. Low and very low birth weight in infants conceived with use of assisted reproductive technology. N Engl J Med. 2002;346:731–7.CrossRefPubMedGoogle Scholar
  10. 10.
    Maher ER, Afnan M, Barratt CL. Epigenetic risks related to assisted reproductive technologies: epigenetics, imprinting, ART and icebergs? Hum Reprod. 2003;18:2508–11.CrossRefPubMedGoogle Scholar
  11. 11.
    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;17:22–9.CrossRefPubMedGoogle Scholar
  12. 12.
    Eroglu A, Layman LC. Role of ART in imprinting disorders. Semin Reprod Med. 2012;30:92–104.Google Scholar
  13. 13.
    Manipalviratn S, DeCherney A, Segars J. Imprinting disorders and assisted reproductive technology. Fertil Steril. 2009;91:305–15.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Horsthemke B, Wagstaff J. Mechanisms of imprinting of the Prader-Willi/Angelman region. Am J Med Genet A. 2008;146A:2041–52.CrossRefPubMedGoogle Scholar
  15. 15.
    Abu-Amero S, Monk D, Frost J, Preece M, Stanier P, Moore GE. The genetic aetiology of Silver-Russell syndrome. J Med Genet. 2008;45:193–9.CrossRefPubMedGoogle Scholar
  16. 16.
    DeBaun MR, Niemitz EL, Feinberg AP. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am J Hum Genet. 2003;72:156–60.CrossRefPubMedGoogle Scholar
  17. 17.
    Gicquel C, Gaston V, Mandelbaum J, Siffroi JP, Flahault A, Le Bouc Y. 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;72:1338–41.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Maher ER, Brueton LA, Bowdin SC, Luharia A, Cooper W, Cole TR, et al. Beckwith-Wiedemann syndrome and assisted reproduction technology (ART). J Med Genet. 2003;40:62–4.Google Scholar
  19. 19.
    Jirtle RL. Imprinted gene databases. http://geneimprint.com/site/genes-by-species.Homo+sapiens.imprinted-All. Accessed on May 10, 2017. 2017.
  20. 20.
    Pandey S, Shetty A, Hamilton M, Bhattacharya S, Maheshwari A. Obstetric and perinatal outcomes in singleton pregnancies resulting from IVF/ICSI: a systematic review and meta-analysis. Hum Reprod Update. 2012;18:485–503.CrossRefPubMedGoogle Scholar
  21. 21.
    Cortessis VK. Imprinting errors and IVF. In: Van Voorhis BJ, editor. Biennial review of infertility. Dordrecht: Springer; 2009. p. 239–46.CrossRefGoogle Scholar
  22. 22.
    Vermeiden JP, Bernardus RE. Are imprinting disorders more prevalent after human in vitro fertilization or intracytoplasmic sperm injection? Fertil Steril. 2013;99:642–51.CrossRefPubMedGoogle Scholar
  23. 23.
    Lazaraviciute G, Kauser M, Bhattacharya S, Haggarty P, Bhattacharya S. A systematic review and meta-analysis of DNA methylation levels and imprinting disorders in children conceived by IVF/ICSI compared with children conceived spontaneously. Hum Reprod Update. 2014;20:840–52.CrossRefPubMedGoogle Scholar
  24. 24.
    Lazaraviciute G, Kauser M, Bhattacharya S, Haggarty P, Bhattacharya S. A systematic review and meta-analysis of DNA methylation levels and imprinting disorders in children conceived by IVF/ICSI compared with children conceived spontaneously. Hum Reprod Update. 2015;21:555–7.CrossRefPubMedGoogle Scholar
  25. 25.
    Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG. Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42:377–81.CrossRefPubMedGoogle Scholar
  26. 26.
    Gold JA, Ruth C, Osann K, Flodman P, McManus B, Lee HS, et al. Frequency of Prader-Willi syndrome in births conceived via assisted reproductive technology. Genet Med. 2014;16:164–9.Google Scholar
  27. 27.
    Hiura H, Okae H, Miyauchi N, Sato F, Sato A, van de Pette M, et al. Characterization of DNA methylation errors in patients with imprinting disorders conceived by assisted reproduction technologies. Hum Reprod. 2012;27(8):2541–8.Google Scholar
  28. 28.
    Sweeting MJ, Sutton AJ, Lambert PC. What to add to nothing? Use and avoidance of continuity corrections in meta-analysis of sparse data. Stat Med. 2004;23:1351–75.CrossRefPubMedGoogle Scholar
  29. 29.
    Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–58.CrossRefPubMedGoogle Scholar
  30. 30.
    Doornbos ME, Maas SM, McDonnell J, Vermeiden JP, Hennekam RC. Infertility, assisted reproduction technologies and imprinting disturbances: a Dutch study. Hum Reprod. 2007;22:2476–80.CrossRefPubMedGoogle Scholar
  31. 31.
    Halliday J, Oke K, Breheny S, Algar E, JA D. Beckwith-Wiedemann syndrome and IVF: a case-control study. Am J Hum Genet. 2004;75:526–8.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Kallen B, Finnstrom O, Nygren KG, Olausson PO. In vitro fertilization (IVF) in Sweden: risk for congenital malformations after different IVF methods. Birth Defects Res Part A Clin Molec Teratol. 2005;73:162–9.CrossRefGoogle Scholar
  33. 33.
    Lidegaard O, Pinborg A, Andersen AN. Imprinting diseases and IVF: Danish National IVF cohort study. Hum Reprod. 2005;20(4):950–4.CrossRefPubMedGoogle Scholar
  34. 34.
    Marees T, Dommering CJ, Imhof SM, Kors WA, Ringens PJ, van Leeuwen FE, et al. Incidence of retinoblastoma in Dutch children conceived by IVF: an expanded study. Hum Reprod. 2009;24:3220–4.Google Scholar
  35. 35.
    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;49:129–34.CrossRefPubMedGoogle Scholar
  36. 36.
    Sutcliffe AG, Peters CJ, Bowdin S, Temple K, Reardon W, Wilson L, et al. Assisted reproductive therapies and imprinting disorders—a preliminary British survey. Hum Reprod. 2006;21:1009–11.Google Scholar
  37. 37.
    Wilkins-Haug L, Porter A, Hawley P, Benson CB. Isolated fetal omphalocele, Beckwith-Wiedemann syndrome, and assisted reproductive technologies. Birth Defects Res A Clin Mol Teratol. 2009;85:58–62.CrossRefPubMedGoogle Scholar
  38. 38.
    Chiba H, Hiura H, Okae H et al. DNA methylation errors in imprinting disorders and assisted reproductive technology. Pediatr Int. 2013;55:542–9.Google Scholar
  39. 39.
    Pinborg A, Loft A, Romundstad LB, Wennerholm UB, Söderström-Anttila V, Bergh C, et al. Epigenetics and assisted reproductive technologies. Acta Obstet Gynecol Scand. 2016;95:10–5.Google Scholar
  40. 40.
    Hoeijmakers L, Kempe H, Verschure PJ. Epigenetic imprinting during assisted reproductive technologies: the effect of temporal and cumulative fluctuations in methionine cycling on the DNA methylation state. Mol Reprod Dev. 2016;83:94–107.CrossRefPubMedGoogle Scholar
  41. 41.
    Houshdaran S, Cortessis VK, Siegmund K, Yang A, Laird PW, Sokol RZ. Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS One. 2007;2:e1289.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Eggermann T, Netchine I, Temple IK, Tümer Z, Monk D, Mackay D, et al. Congenital imprinting disorders: EUCID.net—a network to decipher their aetiology and to improve the diagnostic and clinical care. Clin Epigenetics. 2015;7:23.Google Scholar
  43. 43.
    Conlin LK, Thiel BD, Bonnemann CG, Medne L, Ernst LM, Zackai EH, et al. Mechanisms of mosaicism, chimerism and uniparental disomy identified by single nucleotide polymorphism array analysis. Hum Mol Genet. 2010;19:1263–75.Google Scholar
  44. 44.
    Snijders RJ, Sundberg K, Holzgreve W, Henry G, Nicolaides KH. Maternal age- and gestation-specific risk for trisomy 21. Ultrasound Obstet Gynecol. 1999;13:167–70.CrossRefPubMedGoogle Scholar
  45. 45.
    Zaslav AL, Fallet S, Brown S, Ebert R, Fleischer A, Valderama E, et al. Prenatal diagnosis of low level trisomy 15 mosaicism: review of the literature. Clin Genet. 1998;53:286–92.Google Scholar
  46. 46.
    Christian SL, Smith AC, Macha M, et al. Prenatal diagnosis of uniparental disomy 15 following trisomy 15 mosaicism. Prenat Diagn. 1996;16:323–32.CrossRefPubMedGoogle Scholar
  47. 47.
    Chen CP, Chern SR, Chen YN, Wu PS, Yang CW, Chen LF, et al. Mosaic trisomy 15 at amniocentesis: prenatal diagnosis, molecular genetic analysis and literature review. Taiwan J Obstet Gynecol. 2015;54:426–31.Google Scholar
  48. 48.
    Robinson WP, Bottani A, Xie YG, Balakrishman J, Binkert F, Mächler M, et al. Molecular, cytogenetic, and clinical investigations of Prader-Willi syndrome patients. Am J Hum Genet. 1991;49:1219–34.Google Scholar
  49. 49.
    Mitchell J, Schinzel A, Langlois S, Gillessen-Kaesbach G, Schuffenhauer S, Michaelis R, et al. Comparison of phenotype in uniparental disomy and deletion Prader-Willi syndrome: sex specific differences. Am J Med Genet. 1996;65:133–6.Google Scholar
  50. 50.
    Sartorelli EM, Mazzucatto LF, de Pina-Neto JM. Effect of paternal age on human sperm chromosomes. Fertil Steril. 2001;76:1119–23.CrossRefPubMedGoogle Scholar
  51. 51.
    Wiener-Megnazi Z, Auslender R, Dirnfeld M. Advanced paternal age and reproductive outcome. Asian J Androl. 2012;14:69–76.CrossRefPubMedGoogle Scholar
  52. 52.
    Sandin S, Schendel D, Magnusson P, Hultman C, Surén P, Susser E, et al. Autism risk associated with parental age and with increasing difference in age between the parents. Mol Psychiatry. 2016;21:693–700.Google Scholar
  53. 53.
    Docherty LE, Rezwan FI, Poole RL, et al. Mutations in NLRP5 are associated with reproductive wastage and multilocus imprinting disorders in humans. Nat Commun. 2015;6:8086.  https://doi.org/10.1038/ncomms9086.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Centers for Disease Control and Prevention, American Society for Reproductive Medicine, Technology SfAR. Assisted Reproductive Technology National Summary Report 2014. Atlanta: US Dept of Health and Human Services; 2016.Google Scholar
  55. 55.
    United Nations Statistics Division. United Nations report on vital statistics, Series A, Vol LVIII, No 1, 2006.Google Scholar
  56. 56.
    Chambers GM, Sullivan EA, Ishihara O, Chapman MG, Adamson GD. The economic impact of assisted reproductive technology: a review of selected developed countries. Fertil Steril. 2009;91:2281–94.CrossRefPubMedGoogle Scholar
  57. 57.
    Irahara M, Kuwahara A, Iwasa T, Ishikawa T, Ishihara O, Kugu K, et al. Assisted reproductive technology in Japan: a summary report of 1992–2014 by the Ethics Committee, Japan Society of Obstetrics and Gynecology. Reprod Med Biol. 2017;16:126–32.Google Scholar
  58. 58.
    Kultursay N, Senrencber S, Arcasoy M, Capanoglu R, Yuce G. DiGeorge syndrome after in vitro fertilization. J Assist Reprod Genet. 1993;10:380–1.CrossRefPubMedGoogle Scholar
  59. 59.
    Sutcliffe AG, D'Souza SW, Cadman J, Richards B, McKinlay IA, Lieberman B. Minor congenital anomalies, major congenital malformations and development in children conceived from cryopreserved embryos. Hum Reprod. 1995;10:3332–7.CrossRefPubMedGoogle Scholar
  60. 60.
    Koudstaal J, Braat DD, Bruinse HW, Naaktgeboren N, Vermeiden JP, Visser GH. Obstetric outcome of singleton pregnancies after IVF: a matched control study in four Dutch university hospitals. Hum Reprod. 2000;15:1819–25.CrossRefPubMedGoogle Scholar
  61. 61.
    Olivennes F, Mannaerts B, Struijs M, Bonduelle M, Devroey P. Perinatal outcome of pregnancy after GnRH antagonist (ganirelix) treatment during ovarian stimulation for conventional IVF or ICSI: a preliminary report. Hum Reprod. 2001;16:1588–91.CrossRefPubMedGoogle Scholar
  62. 62.
    Orstavik KH. Intracytoplasmic sperm injection and congenital syndromes because of imprinting defects. Tidsskr Nor Laegeforen. 2003;123:177.PubMedGoogle Scholar
  63. 63.
    Ludwig M, Katalinic A, Gross S, Sutcliffe A, Varon R, Horsthemke B. Increased prevalence of imprinting defects in patients with Angelman syndrome born to subfertile couples. J Med Genet. 2005;42:289–91.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Lidegaard O, Pinborg A, Andersen AN. Imprinting disorders after assisted reproductive technologies. Curr Opin Obstet Gynecol. 2006;18:293–6.CrossRefPubMedGoogle Scholar
  65. 65.
    Bowdin S, Allen C, Kirby G, Brueton L, Afnan M, Barratt C, et al. A survey of assisted reproductive technology births and imprinting disorders. Hum Reprod. 2007;22:3237–40.Google Scholar
  66. 66.
    Kagami M, Nagai T, Fukami M, Yamazawa K, Ogata T. Silver-Russell syndrome in a girl born after in vitro fertilization: partial hypermethylation at the differentially methylated region of PEG1/MEST. J Assist Reprod Genet. 2007;24:131–6.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Lim D, Bowdin SC, Tee L, et al. Clinical and molecular genetic features of Beckwith-Wiedemann syndrome associated with assisted reproductive technologies. Hum Reprod. 2009;24:741–7.CrossRefPubMedGoogle Scholar
  68. 68.
    King JL, Yang B, Sparks AE, Mains LM, Murray JC, Van Voorhis BJ. Skewed X inactivation and IVF-conceived infants. Reprod BioMed Online. 2010;20:660–3.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Kuentz P, Bailly A, Faure AC, Blagosklonov O, Amiot C, Bresson JL, et al. Child with Beckwith-Wiedemann syndrome born after assisted reproductive techniques to an human immunodeficiency virus serodiscordant couple. Fertil Steril. 2011;96:e35–8.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Victoria K. Cortessis
    • 1
    • 2
    Email author
  • Moosa Azadian
    • 1
  • James Buxbaum
    • 3
  • Fatimata Sanogo
    • 1
  • Ashley Y. Song
    • 1
  • Intira Sriprasert
    • 1
  • Pengxiao C. Wei
    • 1
  • Jing Yu
    • 1
  • Karine Chung
    • 2
  • Kimberly D. Siegmund
    • 1
  1. 1.Department of Preventive MedicineKeck School of Medicine at USCLos AngelesUSA
  2. 2.Department of Obstetrics and GynecologyKeck School of Medicine at USCLos AngelesUSA
  3. 3.Department of MedicineKeck School of Medicine at USCLos AngelesUSA

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