Reproductive BioMedicine Online
Volume 20, Issue 2 , Pages 191-200 , February 2010

Miscarriage risk for IVF pregnancies in poor responders to ovarian hyperstimulation

  • Maaike L Haadsma

      Affiliations

    • Department of Obstetrics and Gynaecology, University Medical Center Groningen, University of Groningen, PO Box 30.001, 9700 RB Groningen, The Netherlands
    • Department of Genetics, University Medical Center Groningen, University of Groningen, PO Box 30.001, 9700 RB Groningen, The Netherlands
    • Corresponding Author InformationCorresponding author.
    • ,
  • Henk Groen

      Affiliations

    • Department of Epidemiology, University Medical Center Groningen, University of Groningen, PO Box 30.001, 9700 RB Groningen, The Netherlands
    • ,
  • Thea M Mooij

      Affiliations

    • Department of Epidemiology, Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
    • ,
  • Curt W Burger

      Affiliations

    • Department of Obstetrics and Gynaecology, Erasmus Medical Center Rotterdam, PO Box 2040, 3000 CA Rotterdam, The Netherlands
    • ,
  • Frank JM Broekmans

      Affiliations

    • Department of Reproductive Medicine and Gynaecology, University Medical Center Utrecht, PO Box 85500, 3508 GA Utrecht, The Netherlands
    • ,
  • Cornelis B Lambalk

      Affiliations

    • Department of Obstetrics and Gynaecology, Vrije Universiteit Medical Center, PO Box 7057, 1007 MB Amsterdam, The Netherlands
    • ,
  • Flora E van Leeuwen

      Affiliations

    • Department of Epidemiology, Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
    • ,
  • Annemiek Hoek

      Affiliations

    • Department of Obstetrics and Gynaecology, University Medical Center Groningen, University of Groningen, PO Box 30.001, 9700 RB Groningen, The Netherlands
    • ,
  • on behalf of The OMEGA Project Group

      Affiliations

    • R Schats (Vrije Universiteit Medical Center Amsterdam), NS Macklon (University Medical Center Utrecht), JSE Laven (Erasmus Medical Center Rotterdam), CAM Jansen (Diaconessenhuis Voorburg), FM Helmerhorst, N Naaktgeboren (Leiden University Medical Center), BJ Cohlen (Isala Clinics Zwolle), DDM Braat, JAM Kremer, WNP Willemsen (Radboud University Nijmegen Medical Center), RSGM Bots (St Elisabeth Hospital Tilburg), AHM Simons (University Medical Center Groningen), F van der Veen (Academic Medical Center Amsterdam), JLH Evers (Academic Hospital Maastricht), and PA van Dop (Catharina Hospital Eindhoven).

Received 10 April 2009 ,Revised 26 May 2009 ,Accepted 14 October 2009.

References 

  1. Abdalla H, Thum MY. An elevated basal FSH reflects a quantitative rather than qualitative decline of the ovarian reserve. Hum. Reprod. 2004;19:893–898
  2. Baird DT, Collins J, Egozcue J, et al. Fertility and ageing. Hum. Reprod. Update. 2005;11:261–276
  3. Bancsi LF, Broekmans FJ, Looman CW, et al. Impact of repeated antral follicle counts on the prediction of poor ovarian response in women undergoing in vitro fertilization. Fertil. Steril. 2004;81:35–41
  4. Block E. Quantitative morphological investigations of the follicular system in women; variations at different ages. Acta Anat. 1952;14:108–123
  5. Boue A, Boue J, Gropp A. Cytogenetics of pregnancy wastage. Adv. Hum. Genet. 1985;14:1–57
  6. Brigham SA, Conlon C, Farquharson RG. A longitudinal study of pregnancy outcome following idiopathic recurrent miscarriage. Hum. Reprod. 1999;14:2868–2871
  7. Broekmans FJ, Kwee J, Hendriks DJ. A systematic review of tests predicting ovarian reserve and IVF outcome. Hum. Reprod. Update. 2006;12:685–718
  8. de Boer EJ, den Tonkelaar I, Te Velde ER, et al. Increased risk of early menopausal transition and natural menopause after poor response at first IVF treatment. Hum. Reprod. 2003;18:1544–1552
  9. de Koning CH, Benjamins T, Harms P. The distribution of FSH receptor isoforms is related to basal FSH levels in subfertile women with normal menstrual cycles. Hum. Reprod. 2006;21:443–446
  10. de Koning CH, Popp-Snijders C, Martens F, et al. Falsely elevated follicle-stimulating hormone levels in women with regular menstrual cycles due to interference in immunoradiometric assay. J. Assist. Reprod. Genet. 2000;17:457–459
  11. de Sutter P, Dhont M. Poor response after hormonal stimulation for in vitro fertilization is not related to ovarian aging. Fertil. Steril. 2003;79:1294–1298
  12. Dursun P, Gultekin M, Yuce K, et al. What is the underlying aneuploidy associated cause of with increasing maternal age? Is it associated with elevated levels of gonadotropins?. Med. Hypotheses. 2005;66:143–147
  13. Eichenlaub-Ritter U. Genetics of oocyte ageing. Maturitas. 1998;30:143–169
  14. Elter K, Kavak ZN, Gokaslan H, et al. Antral follicle assessment after down-regulation may be a useful tool for predicting pregnancy loss in in vitro fertilization pregnancies. Gynecol. Endocrinol. 2005;21:33–37
  15. Gaulden ME. Maternal age effect: the enigma of Down syndrome and other trisomic conditions. Mutat. Res. 1992;296:69–88
  16. Gosden RG, Faddy MJ. Ovarian aging, follicular depletion, and steroidogenesis. Exp. Gerontol. 1994;29:265–274
  17. Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr. Rev. 1996;17:121–155
  18. Gougeon A, Ecochard R, Thalabard JC. Age-related changes of the population of human ovarian follicles: increase in the disappearance rate of non-growing and early-growing follicles in aging women. Biol. Reprod. 1994;50:653–663
  19. Haadsma ML, Groen H, Fidler V, et al. The predictive value of ovarian reserve tests for spontaneous pregnancy in subfertile ovulatory women. Hum. Reprod. 2008;23:1800–1807
  20. Haadsma ML, Groen H, Fidler V, et al. The predictive value of ovarian reserve tests for miscarriage in a population of subfertile ovulatory women. Hum. Reprod. 2009;24:546–552
  21. Hanoch J, Lavy Y, Holzer H, et al. Young low responders protected from untoward effects of reduced ovarian response. Fertil. Steril. 1998;69:1001–1004
  22. Hansen KR, Knowlton NS, Thyer AC, et al. A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum. Reprod. 2008;23:699–708
  23. Hassold T, Hunt P. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2001;2:280–291
  24. Hassold T, Abruzzo M, Adkins K, et al. Human aneuploidy: incidence, origin, and etiology. Environ. Mol. Mutagen. 1996;28:167–175
  25. Havryliuk Y, Dragisic KG, Rosenwaks Z. Baseline serum FSH levels in poor prognostic IVF patients: do abnormal levels predict fetal aneuploidy?. Fertil. Steril. 2006;86:S21
  26. Henderson SA, Edwards RG, et al. Chiasma frequency and maternal age in mammals. Nature. 1968;218:22–28
  27. Hendriks DJ, Te Velde ER, Looman CW, et al. Expected poor ovarian response in predicting cumulative pregnancy rates: a powerful tool. Reprod. Biomed. Online. 2008;17:727–736
  28. Hunt PA, Hassold TJ. Human female meiosis: what makes a good egg go bad?. Trends Genet. 2008;24:86–93
  29. Klinkert ER, Broekmans FJ, Looman CW, et al. A poor response in the first in vitro fertilization cycle is not necessarily related to a poor prognosis in subsequent cycles. Fertil. Steril. 2004;81:1247–1253
  30. Klip H, van Leeuwen FE, Schats R, et al. Risk of benign gynecological diseases and hormonal disorders according to responsiveness to ovarian stimulation in IVF: a follow-up study of 8714 women. Hum. Reprod. 2003;18:1951–1958
  31. Kumbak B, Ulug U, Erzik B, et al. Early clinical pregnancy loss rate in poor responder patients does not change compared to age-matched normoresponders. Fertil. Steril. 2008;91:106–109
  32. Lambalk CB, de Koning CH. Interpretation of elevated FSH in the regular menstrual cycle. Maturitas. 1998;30:215–220
  33. Lambers MJ, Mager E, Goutbeek J, et al. Factors determining early pregnancy loss in singleton and multiple implantations. Hum. Reprod. 2007;22:275–279
  34. Lawson R, El-Toukhy T, Kassab A, et al. Poor response to ovulation induction is a stronger predictor of early menopause than elevated basal FSH: a life table analysis. Hum. Reprod. 2003;18:527–533
  35. Lekamge DN, Barry M, Kolo M, et al. Anti-Mullerian hormone as a predictor of IVF outcome. Reprod. Biomed. Online. 2007;14:602–610
  36. Levi AJ, Raynault MF, Bergh PA, et al. Reproductive outcome in patients with diminished ovarian reserve. Fertil. Steril. 2001;76:666–669
  37. Lintsen AM, Pasker-de Jong PC, de Boer EJ, et al. Effects of subfertility cause, smoking and body weight on the success rate of IVF. Hum. Reprod. 2005;20:1867–1875
  38. Luna M, Grunfeld L, Mukherjee T, et al. Moderately elevated levels of basal follicle-stimulating hormone in young patients predict low ovarian response, but should not be used to disqualify patients from attempting in vitro fertilization. Fertil. Steril. 2007;87:782–787
  39. Maheshwari A, Fowler P, Bhattacharya S. Assessment of ovarian reserve–should we perform tests of ovarian reserve routinely?. Hum. Reprod. 2006;21:2729–2735
  40. Massie JA, Burney RO, Milki AA, et al. Basal follicle-stimulating hormone as a predictor of fetal aneuploidy. Fertil. Steril. 2008;90:2351–2355
  41. McTavish KJ, Jimenez M, Walters KA, et al. Rising follicle-stimulating hormone levels with age accelerate female reproductive failure. Endocrinology. 2007;148:4432–4439
  42. Moreno C, Ruiz A, Simon C, et al. Intracytoplasmic sperm injection as a routine indication in low responder patients. Hum. Reprod. 1998;13:2126–2129
  43. Nasseri A, Mukherjee T, Grifo JA, et al. Elevated day 3 serum follicle stimulating hormone and/or estradiol may predict fetal aneuploidy. Fertil. Steril. 1999;71:715–718
  44. Nikolaou D, Templeton A. Early ovarian ageing. Eur. J. Obstet. Gynecol. Reprod. Biol. 2004;113:126–133
  45. Nybo Andersen AM, Wohlfahrt J, Christens P, et al. Maternal age and fetal loss: population based register linkage study. BMJ. 2000;320:1708–1712
  46. Quenby S, Vince G, Farquharson R, et al. Recurrent miscarriage: a defect in nature’s quality control?. Hum. Reprod. 2002;17:1959–1963
  47. Rothman KJ, Greenland S. Introduction to stratified analysis. In: Modern Epidemiology. Philadelphia: Lippincott-Raven; 1998;p. 256–258
  48. Sabatini L, Zosmer A, Hennessy EM, et al. Relevance of basal serum FSH to IVF outcome varies with patient age. Reprod. Biomed. Online. 2008;17:10–19
  49. Saldeen P, Kallen K, Sundstrom P. The probability of successful IVF outcome after poor ovarian response. Acta Obstet. Gynecol. Scand. 2007;86:457–461
  50. Shanbhag S, Aucott L, Bhattacharya S et al. 2007 Interventions for ‘poor responders’ to controlled ovarian hyperstimulation (COH) in in-vitro fertilisation (IVF). Cochrane Database of Systematic Reviews, CD004379.
  51. Tarin JJ. Aetiology of age-associated aneuploidy: a mechanism based on the ‘free radical theory of ageing’. Hum. Reprod. 1995;10:1563–1565
  52. Tarlatzis BC, Zepiridis L, Grimbizis G, et al. Clinical management of low ovarian response to stimulation for IVF: a systematic review. Hum. Reprod. Update. 2003;9:61–76
  53. Te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum. Reprod. Update. 2002;8:141–154
  54. Te Velde ER, Dorland M, Broekmans FJ. Age at menopause as a marker of reproductive ageing. Maturitas. 1998;30:119–125
  55. Tummers P, De Sutter P, Dhont M. Risk of spontaneous abortion in singleton and twin pregnancies after IVF/ICSI. Hum. Reprod. 2003;18:1720–1723
  56. van Blerkom J, Antczak M, Schrader R. The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum. Reprod. 1997;12:1047–1055
  57. van der Steeg JW, Steures P, Eijkemans MJ, et al. Predictive value and clinical impact of Basal follicle-stimulating hormone in subfertile, ovulatory women. J. Clin. Endocrinol. Metab. 2007;92:2163–2168
  58. van Montfrans JM, van Hooff MH, Huirne JA, et al. Basal FSH concentrations as a marker of ovarian ageing are not related to pregnancy outcome in a general population of women over 30 years. Hum. Reprod. 2004;19:430–434
  59. van Rooij I, Broekmans FJ, Hunault CC, et al. Use of ovarian reserve tests for the prediction of ongoing pregnancy in couples with unexplained or mild male infertility. Reprod. Biomed. Online. 2006;12:182–190
  60. Warburton D. The effect of maternal age on the frequency of trisomy: change in meiosis or in utero selection?. Prog. Cell Cycle Res. 1989;311:165–181
  61. Warburton D. Biological aging and the etiology of aneuploidy. Cytogenet. Genome Res. 2005;111:266–272
  62. Winter E, Wang J, Davies MJ, Norman R. Early pregnancy loss following assisted reproductive technology treatment. Hum. Reprod. 2002;17:3220–3223
  63. Zhen XM, Qiao J, Li R, Wang LN, et al. The clinical analysis of poor ovarian response in in-vitro-fertilization embryo-transfer among Chinese couples. J. Assist. Reprod. Genet. 2008;25:17–22

 Maaike Haadsma graduated from the Faculty of Medicine of the University of Groningen, the Netherlands. In 2004 she joined the department of Obstetrics and Gynaecology of the University Medical Center Groningen, the Netherlands, where she started her research in the field of ovarian ageing. In March 2010 she will defend her PhD thesis on the clinical relation between oocyte quantity and oocyte quality. Maaike Haadsma is currently working as a clinical geneticist in training at the department of Genetics in the same hospital.

PII: S1472-6483(09)00218-1

doi: 10.1016/j.rbmo.2009.11.005

Reproductive BioMedicine Online
Volume 20, Issue 2 , Pages 191-200 , February 2010

Article Tools

* Image Usage & Resolution