Skip to main content

Advertisement

SpringerLink
Log in

Fertility preservation for genetic diseases leading to premature ovarian insufficiency (POI)

  • Review
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

The current review aims to summarize the data available concerning the applicability of fertility preservation techniques to genetic conditions at risk of premature ovarian insufficiency (POI).

Methods

A literature review through the PubMed Database was carried out.

Results

About 10% of cases of POI is related to genetic diseases. The most frequent conditions associated with POI are Turner syndrome and fragile X pre-mutation; mutation of BRCA 1-2 genes and several other mutations and genetic syndromes have recently been highlighted, although they rarely occur. If a diagnosis is issued before POI onset, counseling on currently available fertility preservation techniques is advisable. In case of spontaneous menarche (this can occur variably depending on the mutation) established techniques like embryo or oocyte cryopreservation can be proposed, even if, in some cases, their effectiveness may be reduced by ovarian alterations connected to the mutation. Ovarian tissue cryopreservation has recently been defined as an established medical procedure for fertility preservation in young cancer patients and may be an option for prepubertal patients. However, it is still experimental in special populations with genetic diseases causing POI. New innovative experimental techniques, like in vitro maturation of immature oocytes (IVM) and vitro activation (IVA) of immature follicles on ovarian tissue, have shown limited but encouraging data and they will be probably available in the near future. For a correct risk-benefit evaluation, the following aspects should be considered: actual knowledge about the pathology-specific efficacy of the various techniques, the average age of onset of POI, the possible risks associated with the procedure in relation to the underlying pathology, the probability of spontaneous conception, as well as the health implications of a possible future pregnancy..

Conclusions

Fertility preservation techniques represent a crucial opportunity for patients with genetic risk of POI. Early diagnosis increases the chances to apply these techniques. No specific recommendations concerning fertility preservation for each genetic pathology are available, and clinicians should first counsel the patient and her relatives about known risks and benefits of the available techniques, both those established and those considered as experimental.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Not applicable

References

  1. European Society for Human Reproduction and Embryology (ESHRE) Guideline Group on POI, Webber L, Davies M, Anderson R, Bartlett J, Braat D, et al. ESHRE Guideline: management of women with premature ovarian insufficiency. Hum Reprod. 2016;31:926–37.

    Article  Google Scholar 

  2. Nguyen HH, Milat F, Vincent A. Premature ovarian insufficiency in general practice: meeting the needs of women. Aust Fam Phys 2017. 46:360–6.

  3. Grynberg M, Bidet M, Benard J, Poulain M, Sonigo C, Cédrin-Durnerin I, et al. Fertilitypreservation in Turner syndrome. FertilSteril. 2016;105:13–9.

    Google Scholar 

  4. American College of Obstetricians and Gynecologists (ACOG). Committee opinion no. 605: primary ovarian insufficiency in adolescents and young women. Obstet Gynecol. 2014;124:193–7.

    Article  Google Scholar 

  5. Huhtaniemi I, Hovatta O, La Marca A, Livera G, Monniaux G, Persani L, et al. Advances in the molecular pathophysiology,genetics, and treatment of primary ovarian insufficiency. Trends Endocrinol Metab. 2018;29:400–19.

    Article  CAS  PubMed  Google Scholar 

  6. Oktay K, Bedoschi G, Berkowitz K, Bronson R, Kashani B, McGovern P, et al. Fertility preservation in women with Turner syndrome: a comprehensive review and practical guidelines. J Pediatr Adolesc Gynecol. 2016;29:409–16.

    Article  PubMed  Google Scholar 

  7. Reindollar RH. Turner syndrome: contemporary thoughts and reproductive issues. Semin Reprod Med. 2011;29:342–52.

    Article  PubMed  Google Scholar 

  8. Doger E, Çakıroglu Y, Ceylan Y, Ulak E, Özdamar O, Çalışkan E. Reproductive and obstetric outcomes in mosaic Turner’s syndrome: a cross-sectional study and review of the literature. Reprod Biol Endocrinol. 2015;13:59.

    Article  PubMed  PubMed Central  Google Scholar 

  9. El-Mansoury M, Barrenäs ML, Bryman I, Hanson C, Larsson C, Wilhelmsen LV. Chromosomal mosaicism mitigates stigmata and cardiovascular risk factors in Turner syndrome. ClinEndocrinol (Oxf). 2007;66:744–51.

    Article  CAS  Google Scholar 

  10. Ogata T, Matsuo N. Turner syndrome and female sex chromosome aberrations: deduction of the principal factors involved in the development of clinical features. Hum Genet. 1995;95:607–29.

    Article  CAS  PubMed  Google Scholar 

  11. Borgstrom B, Hreinsson J, Rasmussen C, Sheikhi M, Fried G, Keros V, et al. Fertility preservation in girls with Turner syndrome: prognostic signs of the presence of ovarian follicles. J Clin Endocrinol Metab. 2009;94:74–80.

    Article  PubMed  Google Scholar 

  12. Weiss L. Additional evidence of gradual loss of germ cells in the pathogenesis of streak ovaries in Turner’s syndrome. J Med Gen. 1971;8:540–4.

    Article  CAS  Google Scholar 

  13. Hovatta O. Ovarian function and in vitro fertilization (IVF) in Turner syndrome. Pediatr Endocrinol Rev. 2012;9(Suppl 2):713–7.

    PubMed  Google Scholar 

  14. Pasquino AM, Passeri F, Pucarelli I, Segni M, Municchi G. Spontaneouspubertaldevelopment in Turner’ssyndrome. Italian study group for Turner’s syndrome. J Clin Endocrinol Metab. 1997;82:1810–3.

    CAS  PubMed  Google Scholar 

  15. Sutton EJ, McInerney-Leo A, Bondy CA, Gollust SE, King D, Biesecker B. Turner syndrome: four challenges across the lifespan. Am J Med Genet. 2005;139A:57–66.

    Article  PubMed  Google Scholar 

  16. Singh DN, Hara S, Foster HW, Grimes EM. Reproductive performance in women with sex chromosome mosaicism. Obstet Gynecol. 1980;55:608–11.

    CAS  PubMed  Google Scholar 

  17. Kuo PL, Guo HR. Mechanism of recurrent spontaneous abortions in women with mosaicism of X-chromosome aneuploidies. Fertil Steril. 2004;82:1594–601.

    Article  PubMed  Google Scholar 

  18. Khastgir G, Abdalla H, Thomas A, Korea L, Latarche L, Studd J. Oocyte donation in Turner’s syndrome: an analysis of the factors affecting the outcome. Hum Reprod. 1997;12:279–85.

    Article  CAS  PubMed  Google Scholar 

  19. Lau NM, Huang JYJ, MacDonald S, Elizur S, Gidoni Y, Holzer H, et al. Feasibility of fertility preservation in young females with Turner syndrome. Reprod BioMed Online. 2009;18:290–5.

    Article  PubMed  Google Scholar 

  20. Hagman A, Loft A, Wennerholm UB, Pinborg A, Bergh C, Aittomäki K, et al. Obstetric and neonatal outcome after oocyte donation in 106 women with Turner syndrome: a Nordic cohort study. Hum Reprod. 2013;28:1598–609.

    Article  PubMed  Google Scholar 

  21. The Practice Committee of the American Society for Reproductive Medicine. Increased maternal cardiovascular mortality associated with pregnancy in women with Turner syndrome. Fertil Steril. 2012;97:282–4.

    Google Scholar 

  22. Wong SC, Cheung M, Zacharin M. Aortic dilatation and dissection in Turner syndrome: what we know, what we are unclear about and what we should do in clinical practice? Int J Acolesc Med Health. 2014;26:469–88.

    Article  Google Scholar 

  23. Andre H, Pimentel C, Veau S, Domin-Bernhard M, Letur-Konirsch H, Priou G, et al. Pregnancies and obstetrical prognosis after oocyte donation in Turner syndrome: a multicentric study. Eur J Obstet Gynecol Reprod Biol. 2019;238:73–7.

    Article  PubMed  Google Scholar 

  24. Bodri D, Vernaeve V, Figueras F, Vidal R, Guillen JJ, Coll O. Oocyte donation in patients with Turner's syndrome: a successful technique but with an accompanying high risk of hypertensive disorders during pregnancy. Hum Reprod. 2006;21:829–32.

    Article  CAS  PubMed  Google Scholar 

  25. Karnis MF, Zimon AE, Lalwani SI, Timmreck LS, Klipstein S, Reindollar RH. Risk of death in pregnancy achieved through oocyte donation in patients with Turner syndrome: a national survey. FertilSteril. 2003;80:498–501.

    Google Scholar 

  26. Sullivan SD, Welt C, Sherman S. FMR1 and the continuum of primary ovarian insufficiency. Semin Reprod Med. 2011;29:299–307.

    Article  PubMed  Google Scholar 

  27. Sherman SL. Premature ovarian failure in the fragile X syndrome. Am J Med Genet. 2000;97:189–94.

    Article  CAS  PubMed  Google Scholar 

  28. Wheeler AC, Bailey DB Jr, Berry-Kravis E, Greenberg J, Losh M, Mailick M, et al. Associated features in females with an FMR1 premutation. J Neurodev Disord. 2014;6:30.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Avraham S, Almog B, Reche A, Zakar L, Malcov M, Sokolov A, et al. The ovarian response in fragile X patients and premutation carriers undergoing IVF–PGD: reappraisal. Hum Reprod. 2017;32:1508–11.

    Article  CAS  PubMed  Google Scholar 

  30. Welt CK, Smith PC, Taylor AE. Evidence of early ovarian aging in fragile x premutation carriers. J Clin Endocrinol Metab. 2004;89:4569–74.

    Article  CAS  PubMed  Google Scholar 

  31. Lisik MZ. Abnormal function of ovaries in women carriers of premutation in the FMR1 gene. WiadLek. 2007;60:265–9.

    Google Scholar 

  32. Spath MA, Feuth TB, Allen EG, Smiths AP, Yntema HG, van Kessel AG, et al. Intra-individual stability over time of standardized anti-Mullerian hormone in FMR1 premutation carriers. Hum Reprod. 2011;26:2815–91.

    Article  Google Scholar 

  33. Rohr J, Allen EG, Charen K, Giles J, He W, Dominguez C, et al. Anti-Mullerian hormone indicates early ovarian decline in fragile X mental retardation (FMR1) premutation carriers: a preliminary study. Hum Reprod. 2008;23:1220–5.

    Article  CAS  PubMed  Google Scholar 

  34. Hipp HS, Charen KH, Spencer JB, Allen EG, Sherman SL. Reproductive and gynecologic care of women with fragile X primary ovarian insufficiency (FXPOI). Menopause. 2016;23:993–9.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Allen EG, Sullivan AK, Marcus M, Small C, Dominguez C, Epstein MP, et al. Examination of reproductive aging milestones among women who carry the FMR1 premutation. Hum Reprod. 2007;22:2142–52.

    Article  CAS  PubMed  Google Scholar 

  36. Forges T, Monnier-Barbarino P, Leheup B, Jouvet P. Pathophysiology of impaired ovarian function in galactosaemia. Hum Reprod Update. 2006;12:573–84.

    Article  CAS  PubMed  Google Scholar 

  37. van Erven B, Gubbels CS, van Golde RJ, Dunselman GA, Derhaag JG, de Wert G, et al. Fertility preservation in female classic galactosemia patients. Orphanet J Rare Dis. 2013;8:107.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Suzuki M, West C, Beutler E. Large-scale molecular screening for galactosemia alleles in a pan-ethnic population. Hum Genet. 2001;109:210–5.

    Article  CAS  PubMed  Google Scholar 

  39. Mamsen LS, Kelsey TV, Ernst E, Macklon KT, Lund AM, Andersen CY. Cryopreservation of ovarian tissue may be considered in young girls with galactosemia. J Assist Reprod Genet. 2018;35:1209–17.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Thakur M, Feldman G, Puscheck EE. Primary ovarian insufficiency in classic galactosemia: current understanding and future research opportunities. J Assist Reprod Genet. 2018;35:3–16.

    Article  PubMed  Google Scholar 

  41. Gubbels CS, Land JA, Rubio-Gozalbo ME. Fertility and impact of pregnancies on the mother and child in classic galactosemia. Obstet Gynecol Surv. 2008;63:334–43.

    Article  PubMed  Google Scholar 

  42. Fridovich-Keil JL, Gubbels CS, Spencer JB, Sanders RD, Land JA, Rubio-Gozalbo E. Ovarian function in girls and women with GALT-deficiency galactosemia. J Inherit Metab Dis. 2011;34:357–66.

    Article  CAS  PubMed  Google Scholar 

  43. Berry GT. Galactosemia and Amenorrhea in the Adolescent. Ann N Y Acad Sci. 2008;1135:112–7.

    Article  PubMed  Google Scholar 

  44. Sanders RD, Spencer JB, Epstein MP, Pollak SV, Vardhana PA, Lustbader JW, et al. Biomarkers of ovarian function in girls and women with classic galactosemia. Fertil Steril. 2009;92:344–51.

    Article  CAS  PubMed  Google Scholar 

  45. Spencer JB, Badik JR, Ryan EL, Gleason TJ, Broadaway KA, Epstein MP, et al. Modifiers of ovarian function in girls and women with classic galactosemia. J Clin Endocrinol Metab. 2013;98:E1257–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Waggoner DD, Buist NRM, Donnell GN. Long-term prognosis in galactosaemia: results of a survey of 350 cases. J Inherit Metab Dis. 1999;13:802–18.

    Article  Google Scholar 

  47. Kaufman FR, Kogut MD, Donnell GN, Goebelsmann U, March C, Koch R. Hypergonadotropic hypogonadism in female patients with galactosemia. N Engl J Med. 1981;304:994–8.

    Article  CAS  PubMed  Google Scholar 

  48. Levy HL, Driscoll SG, Porensky RS, Wender DF. Ovarian failure in galactosemia. N Engl J Med. 1984;310:50.

    Article  CAS  PubMed  Google Scholar 

  49. Rubio-Gozalbo ME, Gubbels CS, Bakker JA, Menheere PP, Wodzig WK, Land JA. Gonadal function in male and female patients with classic galactosemia. Hum Reprod. 2010;16:177–88.

    CAS  Google Scholar 

  50. Guerrero NV, Singh RH, Manatunga A, Berry GT, Steiner RD, Elsas LJ. Risk factors for premature ovarian failure in females with galactosemia. J Pediatr. 2000;137:833–41.

    Article  CAS  PubMed  Google Scholar 

  51. van Erven B, Berry GT, Cassiman D, Connolly G, Forga M, Gautschi M, et al. Fertility in adult women with classic galactosemia and primary ovarian insufficiency. Fertil Steril. 2017;108:168–74.

    Article  PubMed  Google Scholar 

  52. Lambertini M, Goldrat O, Toss A, Azim HA Jr, Peccatori FA, Ignatiadis M, et al. Fertility and pregnancy issues in BRCA-mutated breast cancer patients. Cancer Treat Rev. 2017;59:61–70.

    Article  PubMed  Google Scholar 

  53. Roy R, Chun J, Powell SN. BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat Rev Cancer. 2012;12:68–78.

    Article  CAS  Google Scholar 

  54. Kuchenbaecker KB, Hopper JL, Barnes DR, Phillips KA, Mooij TM, Roos-Blom MJ, et al. Risks of breast, ovarian, and contralateral breast cancer for BRCA1 and BRCA2 mutation carriers. JAMA. 2017;317:2402–16.

    Article  CAS  PubMed  Google Scholar 

  55. Chen S, Parmigiani G. Meta-analysis of BRCA1 and BRCA2 penetrance. J Clin Oncol. 2007;25:1329–33.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Grynberg M, Raad J, Comtet M, Vinolas C, Cedrin-Durnerin I, Sonigo C. Fertility preservation in BRCA-mutated women: when and how? Future Oncol. 2018;4:483–90.

    Article  Google Scholar 

  57. Kauff ND, Domchek SM, Friebel TM, Robson ME, Lee J, Garber JE, et al. Risk-reducing salpingo-oophorectomy for the prevention of BRCA1- and BRCA2-associated breast and gynecologic cancer: a multicenter, prospective study. J Clin Oncol. 2008;26:1331–7.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Domchek SM, Friebel TM, Garber JE, Isaacs C, Matloff E, Eeles R, et al. Occult ovarian cancers identified at risk-reducing salpingo-oophorectomy in a prospective color of BRCA1/2 mutation carriers. Breast Cancer Res Treat. 2010;124:195–203.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Domchek SM, Friebel TM, Singer CF, Evans DG, Lynch HT, Isaacs C, et al. Association of risk-reducing surgery in BRCA1 or BRCA2 mutation carriers with cancer risk and mortality. JAMA. 2010;304:967–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Finch A, Valentini A, Greenblatt E, Lynch HT, Ghadirian P, Armel S, et al. Frequency of premature menopause in women who carry a BRCA1 or BRCA2 mutation. Fertil Steril. 2013;99:1724–8.

    Article  CAS  PubMed  Google Scholar 

  61. Lin WT, Beattie M, Chen L, Oktay K, Crawford SL, Gold EB, et al. Comparison of age at natural menopause in BRCA1/2 mutation carriers with a non-clinic-based sample of women in northern California. Cancer. 2013;119:1652–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Rzepka-Gorska I, Tarnowski B, Chudecka-G-laz A, Gorski B, Zielinska D, To-loczko-Grabarek A. Premature menopause in patients with BRCA1 gene mutation. Breast Cancer Res Treat. 2006;100:59–63.

    Article  CAS  PubMed  Google Scholar 

  63. Lin W, Titus S, Moy F, Ginsburg ES, Oktay K. Ovarian aging in women with BRCA germline mutations. J Clin Endocrinol Metab. 2017;102:3839–47.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Titus S, Li F, Stobezki R, Akula K, Unsal E, Jeong K, et al. Impairment of BRCA1-related DNA doublestrand break repair leads to ovarian aging in mice and humans. SciTransl Med. 2013;5:172ra21.

    Google Scholar 

  65. Wang ET, Pisarska MD, Bresee C, Chen YD, Lester J, Afshar Y, et al. BRCA1 germline mutations may be associated with reduced ovarian reserve. Fertil Steril. 2014;102:1723–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Giordano S, Garrett-Mayer E, Mittal N, Smith K, Shulman L, Passaglia C, et al. Association of BRCA1 mutations with impaired ovarian reserve: connection between infertility and breast/ovarian cancer risk. J Adolesc Young Adult Oncol. 2016;5:337–43.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Phillips KA, Collins IM, Milne RL, McLachlan SA, Friedlander M, Hickey M, et al. Anti-Mullerian hormone serum concentrations of women with germline BRCA1 or BRCA2 mutations. Hum Reprod. 2016;31:1126–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Peccatori FA, Mangili G, Bergamini A, Filippi F, Martinelli F, Ferrari F, et al. Fertility preservation in women harboring deleterious BRCA mutations: ready for prime time? Hum Reprod. 2018;33:181–7.

    Article  CAS  PubMed  Google Scholar 

  69. Michaelson-Cohen R, Mor P, Srebnik N, Beller U, Levy-Lahad E, Eldar-Geva T. BRCA mutation carriers do not have compromised ovarian reserve. Int J Gynecol Cancer. 2014;24:233–7.

    Article  PubMed  Google Scholar 

  70. van Tilborg TC, Derks-Smeets IAP, Bos AME, Oosterwijk JC, van Golde RJ, de Die-Smulders CE, et al. Serum AMH levels in healthy women from BRCA1/2 mutated families: are they reduced? Hum Reprod. 2016;31:2651–9.

    Article  PubMed  Google Scholar 

  71. Pal T, Keefe D, Sun P, Narod SA, Hereditary Breast Cancer Clinical Study Group. Fertility in women with BRCA mutations: a case-control study. Fertil Steril. 2010;93:1805–8.

    Article  CAS  PubMed  Google Scholar 

  72. Collins IM, Milne RL, McLachlan SA, Friedlander M, Hickey M, Weideman PC, et al. BRCA1 and BRCA2 mutation carriers have earlier natural menopause than their noncarrier relatives? Results from the Kathleen Cuningham Foundation Consortium for Research into Familial Breast Cancer. J Clin Oncol. 2014;24:233–7.

    Google Scholar 

  73. Nuovo S, Passeri M, Di Benedetto E, Calanchini M, Meldolesi I, Di Giacomo MC, et al. Characterization of endocrine features and genotype-phenotypes correlations in blepharophimosis-ptosis-epicanthus inversus syndrome type 1. J Endocrinol Investig. 2016;39:227–33.

    Article  CAS  Google Scholar 

  74. Pierce SB, Chisholm KM, Lynch ED, Lee MK, Walsh T, Opitz JM, et al. Mutations in mitochondrial histidyl tRNA synthetase HARS2 cause ovarian dysgenesis and sensorineural hearing loss of Perrault syndrome. Proc Natl Acad Sci U S A. 2011;108:6543–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Pierce SB, Gersak K, Michaelson-Cohen R, Walsh T, Lee MK, Malach D, et al. Mutations in LARS2, encoding mitochondrial leucyl-tRNA synthetase, lead to premature ovarian failure and hearing loss in Perrault syndrome. Am J Hum Genet. 2013;92:614–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Pallister PD, Opitz JM. The Perrault syndrome: autosomal recessive ovarian dysgenesis with facultative, non-sex-limited sensorineural deafness. Am J Med Genet. 1979;4:239–46.

    Article  CAS  PubMed  Google Scholar 

  77. Tsui V, Crismani W. The Fanconi anemia pathway and fertility. Trends Genet. 2019;35:199–214.

    Article  CAS  PubMed  Google Scholar 

  78. Yang X, Zhang X, Jiao J, Zhang F, Pan Y, Wang Q, et al. Rare variants in FANCA induce premature ovarian insufficiency. Hum Genet. 2019;138:1227–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Chisholm CA, Bray MJ, Karns LB. Successful pregnancy in a woman with Bloom syndrome. Am J Med Genet. 2001;102:136–8.

    Article  CAS  PubMed  Google Scholar 

  80. Jolly A, Bayram Y, Turan S, Aycan Z, Tos T, Abali ZY, et al. Exome sequencing of a primary ovarian insufficiency cohort reveals common molecular etiologies for a spectrum of disease. J Clin Endocrinol Metab. 2019;104:3049–67.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Wasserman D, Asch A. Reproductive medicine and Turner syndrome: ethical issues. Fertil Steril. 2012;98:792–6.

    Article  PubMed  Google Scholar 

  82. Visser JA, Hokken-Koelega ACS, Zandwijken GRJ, Limacher A, Ranke MB, Fluck CE. Anti-Mullerian hormone levels in girls and adolescents with Turner syndrome are related to karyotype, pubertal development and growth hormone treatment. Hum Reprod. 2013;28:1899–907.

    Article  CAS  PubMed  Google Scholar 

  83. American College of Obstetricians and Gynecologists (ACOG). Committee Opinion No. 584: Oocyte Criopreservation. Obstet Gynecol. 2014;123:221–2.

    Article  Google Scholar 

  84. Kavoussi SK, Fisseh S, Smit YR, Smith GD, Christman GM, Gago LA. Oocyte cryopreservation in a woman with mosaic Turner syndrome: a case report. J Reprod Med. 2008;53:223–6.

    PubMed  Google Scholar 

  85. Balen A, Harris S, Chambers E, Picton H. Conservation of fertility and oocyte genetics in a young woman with mosaic Turner syndrome. BJOG. 2010;117:238–42.

    Article  CAS  PubMed  Google Scholar 

  86. El-Shawarby S, Sharif F, Conway G, Serhal P, Davies M. Oocyte cryopreservation after controlled ovarian hyperstimulation in mosaic Turner syndrome: another fertility preservation option in a dedicated UK clinic. BJOG. 2010;117:234–7.

    Article  CAS  PubMed  Google Scholar 

  87. Oktay K, Rodriguez-Wallberg KA, Sahin G. Fertility preservation by ovarian stimulation and oocyte cryopreservation in a 14-year-old adolescent with Turner syndrome mosaicism and impending premature ovarian failure. Fertil Steril. 2010;94:753.e15–9.

    Article  Google Scholar 

  88. Oktay K, Bedoschi G. Oocyte cryopreservation for fertility preservation in postpubertal female children at risk for premature ovarian failure due to accelerated follicle loss in Turner syndrome or cancer treatments. J Pediatr Adolesc Med. 2014;27:342–6.

    CAS  Google Scholar 

  89. Oktay K, Hourvitz A, Sahin G, Oktem O, Safro B, Cil A, et al. Letrozole reduces estrogen and gonadotropin exposure in women with breast cancer undergoing ovarian stimulation before chemotherapy. J Clin Endocrinol Metab. 2006;91:3885–90.

    Article  CAS  PubMed  Google Scholar 

  90. Ito A, Katagiri Y, Tamaki Y, Fukuda Y, Oji A, Morita M. DuoStim: a new option for fertility preservation for a woman with Turner syndrome. Gynecol Endocrinol. 2020;36:1144–8.

    Article  PubMed  Google Scholar 

  91. Birkebaek N, Crüger D, Hansen J, et al. Fertility and pregnancy outcome in Danish women with Turner syndrome. Clin Genet. 2002;61:34–9.

    Article  Google Scholar 

  92. Tarani L, Lampariello S, Raguso G, Colloridi F, Pucarelli I, Pasquino AM, et al. Pregnancy in patients with Turner’s syndrome: six new cases and review of literature. Gynecol Endocrinol. 1998;12:83–7.

    Article  CAS  PubMed  Google Scholar 

  93. Practice Committees of the American Society for Reproductive Medicine and the Society for Assisted Reproductive Technology. The use of preimplantation genetic testing for aneuploidy (PGT-A): a committee opinion. Fertil Steril. 2018;109:429–36.

    Article  Google Scholar 

  94. Hagen CP, Main KM, Kjaergaard S, Juul A. FSH, LH, Inhibin B and estradiol levels in Turner syndrome depend on age and karyotype: longitudinal study of 70 Turner girls with or without spontaneous puberty. Hum Reprod. 2010;25:3134–41.

    Article  CAS  PubMed  Google Scholar 

  95. Hagen CP, Aksglaede L, Sorensen K, Main KM, Boas M, Cleemann L, et al. Serum levels of anti-Mullerian hormone as a marker of ovarian function in 926 healthy females from birth to adulthood and in 172 Turner syndrome patients. J Clin Endocrinol Metab. 2010;95:5003–10.

    Article  CAS  PubMed  Google Scholar 

  96. Azem F, Brener A, Malinger G, Reches A, Many A, Yogev Y, et al. Bypassing physiological puberty, a novel procedure of oocyte cryopreservation at age 7: a case report and review of the literature. Fertil Steril. 2020;114:374–8.

    Article  CAS  PubMed  Google Scholar 

  97. Reichman DE, Davis OK, Zaninovic N, Rosenwaks Z, Goldschlag DE. Fertility preservation using controlled ovarian hyperstimulation and oocyte cryopreservation in a premenarcheal female with myelodysplastic syndrome. Fertil Steril. 2012;98:1225–8.

    Article  PubMed  Google Scholar 

  98. Practice Committee of the American Society for Reproductive Medicine. Fertility preservation in patients undergoing gonadotoxic therapy or gonadectomy: a committee opinion. Fertil Steril. 2019;112:1022–33.

    Article  Google Scholar 

  99. Hreinsson JG, Otala M, Fridstro M, Borgstro B, Rasmussen C, Lundqvist M, et al. Follicles are found in the ovaries of adolescent girls with Turner’s syndrome. J Clin Endocrinol Metab. 2002;87:3618–23.

    CAS  PubMed  Google Scholar 

  100. Hewitt J, Jayasinghe Y, Amor DJ, Gillam LH, Warne LH, Grover S, et al. Fertility in Turner syndrome. Clin Endocrinol. 2013;79:606–14.

    Google Scholar 

  101. Mamsen LS, Charkiewicz K, Anderson RA, Telfer EE, McLaughlin M, Kelsey TW, et al. Characterization of follicles in girls and young women with Turner syndrome who underwent ovarian tissue cryopreservation. Fertil Steril. 2019;111:1217–25.

    Article  PubMed  Google Scholar 

  102. Uzelac PS, Delaney AA, Christensen GL, Bohler HC, Nakajima ST. Live birth following in vitro maturation of oocytes retrieved from extracorporeal ovarian tissue aspiration and embryo cryopreservation for 5 years. Fertil Steril. 2015;104:1258–60.

    Article  PubMed  Google Scholar 

  103. Prasath EB, Chan ML, Wong WH, Lim CJ, Tharmalingam MD, Hendricks M, et al. First pregnancy and live birth resulting from cryopreserved embryos obtained from in vitro matured oocytes after oophorectomy in an ovarian cancer patient. Hum Reprod. 2014;29:276–8.

    Article  CAS  PubMed  Google Scholar 

  104. Huang JY, Tulandi T, Holzer H, Lau NM, Macdonald S, Tan SL, et al. Cryopreservation of ovarian tissue and in vitro matured oocytes in a female with mosaic Turner syndrome: case report. Hum Reprod. 2008;23:336–9.

    Article  CAS  PubMed  Google Scholar 

  105. Zhai J, Yao G, Dong F, Bu Z, Cheng Y, Sato Y, et al. In Vitro Activation of Follicles and Fresh Tissue Auto-transplantation in Primary Ovarian Insufficiency Patients. J Clin Endocrinol Metab. 2016;101:4405–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Suzuki N, Yoshioka N, Takae S, Sugishita Y, Tamura M, Hashimoto S, et al. Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod. 2015;30:608–15.

    Article  PubMed  Google Scholar 

  107. Cabanes L, Chalas C, Christin-Maitre S, Donadille B, Felten ML, Gaxotte V, et al. Turner syndrome and pregnancy: clinical practice. Recommendations for the management of patients with Turner syndrome before and during pregnancy. Eur J Obstet Gynecol Reprod Biol. 2010;152:18–24.

    Article  PubMed  Google Scholar 

  108. The Practice Committees of the American Society for Reproductive Medicine and the Society for Assisted Reproductive Technology. Mature oocyte cryopreservation: a guideline. Fertil Steril. 2013;99:37–43.

    Article  Google Scholar 

  109. Bibi G, Malcov M, Yuval Y, Reches A, Ben-Yosef D, Almog B, et al. The effect of CGG repeat number on ovarian response among fragile X premutation carriers undergoing preimplantation genetic diagnosis. Fertil Sterill. 2010;94:869–74.

    Article  CAS  Google Scholar 

  110. Elizur SE, Levkovitz O, Derech-Haim S, Dratviman-Storobinsky O, Feldman B, Dor J, et al. Elavated levels of FMR1 mRNA in granulosa cells are associated with low ovarian reserve in FMR1 premutation carriers. PLoS One. 2014;9:e105121.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Forges T, Monnier P, Leheup B, Cheillan D, Brivet M, Barbarino A, et al. Ovarian tissue cryopreservation and subsequent spontaneous pregnancies in a patient with classic galactosemia. Fertil Steril. 2011;95:290.e1–3.

    Article  Google Scholar 

  112. Schadewaldt P, Hammen HW, Kamalanathan L, Wendel U, Schwarz M, Bosch AM, et al. Biochemical monitoring of pregnancy and breast feeding in five patients with classical galactosaemia–and review of the literature. Eur J Pediatr. 2009;168:721–9.

    Article  CAS  PubMed  Google Scholar 

  113. Lee SJ, Schover LR, Partridge AH, Patrizio P, Wallace WH, Hagerty K, et al. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol. 2006;24:2917–31.

    Article  PubMed  Google Scholar 

  114. Lambertini M, Goldrat O, Clatot F, Demeestere I, Awada A. Controversies about fertility and pregnancy issues in young breast cancer patients: current state of the art. Curr Opin Oncol. 2017;29:243–52.

    Article  PubMed  Google Scholar 

  115. Henry NL, Xia R, Schott AF, McConnell D, Banerjee M, Hayes DF. Prediction of Postchemotherapy Ovarian Function UsingMarkers of Ovarian Reserve. Oncologist. 2014;19:68–74.

    Article  CAS  PubMed  Google Scholar 

  116. D’Avila AM, Biolchi V, Capp E, von Eye Corleta H. Age, anti-Müllerian hormone, antral follicles count to predict amenorrhea or oligomenorrhea after chemotherapy with cyclophosphamide. J Ovarian Res. 2015;8:82.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Quinn GP, Vadaparampil ST, Tollin S, Miree CA, Murphy D, Bower B, et al. BRCA carriers’ thoughts on risk management in relation to preimplantation genetic diagnosis and childbearing: when too many choices are just as difficult as none. Fertil Steril. 2010;94:2473–5.

    Article  PubMed  Google Scholar 

  118. Shenfield F, Pennings G, Devroey P, Sureau C, Tarlatzis B, Cohen J. ESHRE ethics task force. Taskforce 5: preimplantation genetic diagnosis. Hum Reprod. 2003;18:649–51.

    Article  CAS  PubMed  Google Scholar 

  119. Derks-Smeets IA, Gietel-Habets JJG, Tibben A, Tjan-Heijnen VC, Meijer-Hoogeveen M, Geraedts JP, et al. Decision-making on preimplantation genetic diagnosis and prenatal diagnosis: a challenge for couples with hereditary breast and ovarian cancer. Hum Reprod. 2014;29:1103–12.

    Article  CAS  PubMed  Google Scholar 

  120. Ormondroyd E, Donnelly L, Moynihan C, Savona C, Bancroft E, Evans DG, et al. Attitudes to reproductive genetic testing in women who had a positive BRCA test before having children: a qualitative analysis. Eur J Hum Genet. 2012;20:4–10.

    Article  PubMed  Google Scholar 

  121. Oktay K, Kim JY, Barad D, Babayev SN. Association of BRCA1 mutations with occult primary ovarian insufficiency: a possible explanation for the link between infertility and breast/ovarian cancer risks. J Clin Oncol. 2010;28:240–4.

    Article  CAS  PubMed  Google Scholar 

  122. Turan V, Bedoschi G, EmirdarV MF, Oktay K. Ovarian stimulation in patients with cancer: impact of letrozole and BRCA mutations on fertility preservation cycle outcomes. Reprod Sci. 2018;25:26–32.

    Article  CAS  PubMed  Google Scholar 

  123. Lambertini M, Goldrat O, Ferreira AR, Dechene J, Azim HA Jr, Desir J, et al. Reproductive potential and performance of fertility preservation strategies in BRCA-mutated breast cancer patients. Ann Oncol. 2018;29:237–43.

    Article  CAS  PubMed  Google Scholar 

  124. Shapira M, Raanan H, Feldman B, Srebnik N, Dereck-Haim S, Manela D, et al. BRCA mutation carriers show normal ovarian response in in vitro fertilization cycles. Fertil Steril. 2015;104:1162–7.

    Article  CAS  PubMed  Google Scholar 

  125. Cobo A, Garcia-Velasco JA, Coello A, Domingo J, Pellicer A, Remohi J. Oocyte vitrification as an efficient option for elective fertility preservation. Fertil Steril. 2016;105:755–64.

    Article  PubMed  Google Scholar 

  126. Cakmak H, Katz A, Cedars MI, Rosen MP. Effective method for emergency fertility preservation: random-start controlled ovarian stimulation. Fertil Steril. 2013;100:1673–80.

    Article  PubMed  Google Scholar 

  127. Qin N, Chen Q, Hong Q, et al. Flexibility in starting ovarian stimulation at different phases of the menstrual cycle for treatment of infertile women with the use of in vitro fertilization or intracytoplasmic sperm injection. Fertil Steril. 2016;106:334–41.e1.

    Article  PubMed  Google Scholar 

  128. Sighinolfi G, Sunkara SK, La Marca A. New strategies of ovarian stimulation based on the concept of ovarian follicular waves: from conventional to random and double stimulation. Reprod BioMed Online. 2018;37:489–97.

    Article  PubMed  Google Scholar 

  129. Kuang Y, Chen Q, Hong Q, Lyu Q, Ai A, Fu Y, et al. Double stimulations during the follicular and luteal phases of poor responders in IVF/ ICSI programmes (Shanghai protocol). Reprod BioMed Online. 2014;29:684–91.

    Article  PubMed  Google Scholar 

  130. Rodriguez-Purata J, Devesa M, Parriego M, Pardos C, Rodriguez I, Polyzos NP, et al. Linking back-to-back stimulation cycles with oral contraceptives or progestins in women undergoing embryo accumulation for preimplantation genetic testing, a retrospective study. Gynecol Endocrinol. 2018;34:955–60.

    Article  CAS  PubMed  Google Scholar 

  131. van den Belt-Dusebout AW, Spaan M, Lambalk CB, Kortman M, Laven JS, van Santbrink EJ, et al. Ovarian stimulation for in vitro fertilization and long-term risk of breast cancer. JAMA. 2016;316:300–12.

    Article  PubMed  Google Scholar 

  132. Gronwald J, Glass K, Rosen B, Karlan B, Tung N, Neuhausen SL, et al. Treatment of infertility does not increase the risk of ovarian cancer among women with a BRCA1 or BRCA2 mutation. Fertil Steril. 2016;105:781–5.

    Article  CAS  PubMed  Google Scholar 

  133. Kotsopoulos J, Lubinski J, Gronwald J, Cybulski C, Demsky R, Neuhausen SL, et al. Factors influencing ovulation and the risk of ovarian cancer in BRCA1 and BRCA2 mutation carriers. Int J Cancer. 2015;137:1136–46.

    Article  CAS  PubMed  Google Scholar 

  134. Kim J, Turan V, Oktay K. Long-term safety of letrozole and gonadotropin stimulation for fertility preservation in women with breast cancer. J Clin Endocrinol Metab. 2016;101:1364–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Lambertini M, Del Mastro L, Pescio MC, Andersen CY, Azim HA Jr, Peccatori FA, et al. Cancer and fertility preservation: international recommendations from an expert meeting. BMC Med. 2016;14:1.

    Article  PubMed  PubMed Central  Google Scholar 

  136. Telfer EE, McLaughlin M. Strategies to support human oocyte development in vitro. Int J Dev Biol. 2012;56:901–7.

    Article  CAS  PubMed  Google Scholar 

  137. Azim HA, Kroman N, Paesmans M, Gelber S, Rotmensz N, Ameye L, et al. Prognostic impact of pregnancy after breast cancer according to estrogen receptor status: a multicenter retrospective study. J Clin Oncol. 2013;31:73–9.

    Article  PubMed  Google Scholar 

  138. Hartman M, Liu J, Czene K, Miao H, Chia KS, Salim A, et al. Birth rates among female cancer survivors: a population-based cohort study in Sweden. Cancer. 2013;119:1892–9.

    Article  PubMed  Google Scholar 

  139. Ives A, Saunders C, Bulsara M, Semmens J. Pregnancy after breast cancer: population based study. BMJ. 2007;334:194.

    Article  PubMed  Google Scholar 

  140. Rosenberg L, Thalib L, Adami HO, Hall P. Childbirth and breast cancer prognosis and breast cancer prognosis. Int J Cancer. 2004;III:772–6.

    Article  Google Scholar 

  141. Valentini A, Lubinski J, Byrski T, Ghadirian P, Moller P, Lynch HT. The impact of pregnancy on breast cancer survival in women who carry a BRCA1 or BRCA2 mutation. Breast Cancer Res Treat. 2013;142:177–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medical and Surgical Sciences for Mother, Child and Adult, University of Modena and Reggio Emilia, Modena, Italy

    Antonio La Marca & Elisa Mastellari

  2. Clinica Eugin Modena, Modena, Italy

    Antonio La Marca

Authors
  1. Antonio La Marca
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisa Mastellari
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AL contributed in literature search and in writing the review; EM contributed in literature search and in writing the review

Corresponding author

Correspondence to Antonio La Marca.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

Not applicable

Consent to participate

Not applicable

Consent for publication

Not applicable

Code availability

Not applicable

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

La Marca, A., Mastellari, E. Fertility preservation for genetic diseases leading to premature ovarian insufficiency (POI). J Assist Reprod Genet 38, 759–777 (2021). https://doi.org/10.1007/s10815-021-02067-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10815-021-02067-7

Keywords

Search

Navigation