Fertility and Sterility
Volume 83, Issue 2 , Pages 291-301 , February 2005

Antral follicle count in the prediction of poor ovarian response and pregnancy after in vitro fertilization: A meta-analysis and comparison with basal follicle-stimulating hormone level

Presented as an oral presentation at the 20th Annual Meeting of the European Society of Human Reproduction and Embryology in Berlin, Germany, June 27–30, 2004.

  • Dave J. Hendriks, M.D.

      Affiliations

    • Department of Reproductive Medicine, Division of Obstetrics, Neonatology and Gynecology, University Medical Center Utrecht, Utrecht, The Netherlands
    • Corresponding Author InformationReprint requests: D. J. Hendriks, M.D., University Medical Center Utrecht, Department of Reproductive Medicine, Division of Obstetrics, Neonatology and Gynecology, Heidelberglaan 100, Utrecht 3584 CX, The Netherlands (FAX: 31-30-2505433
  • ,
  • Ben-Willem J. Mol, Ph.D.

      Affiliations

    • Centre for Reproductive Medicine, Department of Obstetrics and Gynecology, Academic Medical Center, Amsterdam, The Netherlands
  • ,
  • László F.J.M.M. Bancsi, Ph.D.

      Affiliations

    • Department of Reproductive Medicine, Division of Obstetrics, Neonatology and Gynecology, University Medical Center Utrecht, Utrecht, The Netherlands
  • ,
  • Egbert R. te Velde, Ph.D.

      Affiliations

    • Department of Reproductive Medicine, Division of Obstetrics, Neonatology and Gynecology, University Medical Center Utrecht, Utrecht, The Netherlands
  • ,
  • Frank J.M. Broekmans, Ph.D.

      Affiliations

    • Department of Reproductive Medicine, Division of Obstetrics, Neonatology and Gynecology, University Medical Center Utrecht, Utrecht, The Netherlands

Received 14 May 2004 ,Revised 13 August 2004 ,Accepted 13 August 2004.

References 

  1. te Velde ER , Pearson PL . The variability of female reproductive ageing . Hum Reprod Update . 2002;8:141–154
  2. 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
  3. Bancsi LF , Broekmans FJ , Mol BW , Habbema JD , te Velde ER . Performance of basal follicle-stimulating hormone in the prediction of poor ovarian response and failure to become pregnant after in vitro fertilization: a meta-analysis . Fertil Steril . 2003;79:1091–1100
  4. Bukman A , Heineman MJ . Ovarian reserve testing and the use of prognostic models in patients with subfertility . Hum Reprod Update . 2001;7:581–590
  5. Ruess ML , Kline J , Santos R , Levin B , Timor-Tritsch I . Age and the ovarian follicle pool assessed with transvaginal ultrasonography . Am J Obstet Gynecol . 1996;174:624–627
  6. Scheffer GJ , Broekmans FJ , Dorland M , Habbema JD , Looman CW , te Velde ER . Antral follicle counts by transvaginal ultrasonography are related to age in women with proven natural fertility . Fertil Steril . 1999;72:845–851
  7. Tomas C , Nuojua-Huttunen S , Martikainen H . Pretreatment transvaginal ultrasound examination predicts ovarian responsiveness to gonadotrophins in in-vitro fertilization . Hum Reprod . 1997;12:220–223
  8. Chang MY , Chiang CH , Hsieh TT , Soong YK , Hsu KH . Use of the antral follicle count to predict the outcome of assisted reproductive technologies . Fertil Steril . 1998;69:505–510
  9. Lijmer JG, Mol BW, Heisterkamp S, Bonsel GJ, Prins MH, van der Meulen JH, et al. Empirical evidence of design-related bias in studies of diagnostic tests . JAMA . 1999;282:1061–1066
  10. Irwig L, Tosteson AN, Gatsonis C, Lau J, Colditz G, Chalmers TC, et al. Guidelines for meta-analyses evaluating diagnostic tests . Ann Intern Med . 1994;120:667–676
  11. SAS Institute . SAS/STAT user's guide, version 6 . 4th ed. Cary, NC: SAS Institute; 1989; 865–9
  12. Midgette AS , Stukel TA , Littenberg B . A meta-analytic method for summarizing diagnostic test performances: receiver-operating-characteristic-summary point estimates . Med Decis Making . 1993;13:253–257
  13. Moses LE , Shapiro D , Littenberg B . Combining independent studies of a diagnostic test into a summary ROC curve: data-analytic approaches and some additional considerations . Stat Med . 1993;12:1293–1316
  14. Fisch JD , Sher G . The antral follicle count (AFC) correlates with metaphase II oocytes and ART cycle outcome: an update . Fertil Steril . 2002;78(3 Suppl 1):S90
  15. Hsieh YY , Chang CC , Tsai HD . Antral follicle counting in predicting the retrieved oocyte number after ovarian hyperstimulation . J Assist Reprod Genet . 2001;18:320–324
  16. Nahum R , Shifren JL , Chang Y , Leykin L , Isaacson K , Toth TL . Antral follicle assessment as a tool for predicting outcome in IVF—is it a better predictor than age and FSH? . J Assist Reprod Genet . 2001;18:151–155
  17. Ng EH , Tang OS , Ho PC . The significance of the number of antral follicles prior to stimulation in predicting ovarian responses in an IVF programme . Hum Reprod . 2000;15:1937–1942
  18. Sharara FI , McClamrock HD . Antral follicle count and ovarian volume predict IVF outcome . Fertil Steril . 2000;74(3 Suppl 1):S176
  19. Sylvestre CV , Child T , Pirwany I , Tan SL . Baseline ultrasound and serum hormonal prediction of follicular response to gonadotropin stimulation during IVF . Fertil Steril . 2002;78(Suppl 1):S6–S7
  20. Yong PY , Baird DT , Thong KJ , McNeilly AS , Anderson RA . Prospective analysis of the relationships between the ovarian follicle cohort and basal FSH concentration, the inhibin response to exogenous FSH and ovarian follicle number at different stages of the normal menstrual cycle and after pituitary down-regulation . Hum Reprod . 2003;18:35–44
  21. Beckers NG , Macklon NS , Eijkemans MJ , Fauser BC . Women with regular menstrual cycles and a poor response to ovarian hyperstimulation for in vitro fertilization exhibit follicular phase characteristics suggestive of ovarian aging . Fertil Steril . 2002;78:291–297
  22. Chiang CH , Chang MY , Shiau CS , Hou HC , Hsieh TT , Soong YK . Effect of a sonographically diffusely enlarged uterus without distinct uterine masses on the outcome of in vitro fertilization-embryo transfer . J Assist Reprod Genet . 1999;16:369–372
  23. Chiang CH , Hsieh TT , Chang MY , Shiau CS , Hou HC , Hsu JJ , et al.  Prediction of pregnancy rate of in vitro fertilization and embryo transfer in women aged 40 and over with basal uterine artery pulsatility index . J Assist Reprod Genet . 2000;17:409–414
  24. Dumesic DA , Damario MA , Session DR , Famuyide A , Lesnick TG , Thornhill AR , et al.  Ovarian morphology and serum hormone markers as predictors of ovarian follicle recruitment by gonadotropins for in vitro fertilization . J Clin Endocrinol Metab . 2001;86:2538–2543
  25. Ficicioglu C , Kutlu T , Demirbasoglu S , Mulayim B . The role of inhibin B as a basal determinant of ovarian reserve . Gynecol Endocrinol . 2003;17:287–293
  26. Frattarelli JL , Lauria-Costab DF , Miller BT , Bergh PA , Scott RT . Basal antral follicle number and mean ovarian diameter predict cycle cancellation and ovarian responsiveness in assisted reproductive technology cycles . Fertil Steril . 2000;74:512–517
  27. Jarvela IY , Sladkevicius P , Kelly S , Ojha K , Campbell S , Nargund G . Quantification of ovarian power Doppler signal with three-dimensional ultrasonography to predict response during in vitro fertilization . Obstet Gynecol . 2003;102:816–822
  28. Loverro G , Nappi L , Mei L , Giacomoantonio L , Carriero C , Tartagni M . Evaluation of functional ovarian reserve in 60 patients . Reprod Biomed Online . 2003;7:200–204
  29. Pohl M , Hohlagschwandtner M , Obruca A , Poschalko G , Weigert M , Feichtinger W . Number and size of antral follicles as predictive factors in vitro fertilization and embryo transfer . J Assist Reprod Genet . 2000;17:315–318
  30. Popovic-Todorovic B , Loft A , Lindhard A , Bangsboll S , Andersson AM , Andersen AN . A prospective study of predictive factors of ovarian response in ‘standard’ IVF/ICSI patients treated with recombinant FSH (A suggestion for a recombinant FSH dosage normogram) . Hum Reprod . 2003;18:781–787
  31. Sharara FI , McClamrock HD . The effect of aging on ovarian volume measurements in infertile women . Obstet Gynecol . 1999;94:57–60
  32. Huang FJ , Chang SY , Tsai MY , Kung FT , Wu JF , Chang HW . Determination of the efficiency of controlled ovarian hyperstimulation in the gonadotropin-releasing hormone agonist-suppression cycle using the initial follicle count during gonadotropin stimulation . J Assist Reprod Genet . 2001;18:91–96
  33. Bancsi LF , Broekmans FJ , Eijkemans MJ , de Jong FH , Habbema JD , te Velde ER . Predictors of poor ovarian response in in vitro fertilization: a prospective study comparing basal markers of ovarian reserve . Fertil Steril . 2002;77:328–336
  34. Frattarelli JL , Levi AJ , Miller BT , Segars JH . A prospective assessment of the predictive value of basal antral follicles in in vitro fertilization cycles . Fertil Steril . 2003;80:350–355
  35. Kupesic S , Kurjak A , Bjelos D , Vujisic S . Three-dimensional ultrasonographic ovarian measurements and in vitro fertilization outcome are related to age . Fertil Steril . 2003;79:190–197
  36. Bancsi LF , Huijs AM , den Ouden CT , Broekmans FJ , Looman CW , Blankenstein MA , et al.  Basal follicle-stimulating hormone levels are of limited value in predicting ongoing pregnancy rates after in vitro fertilization . Fertil Steril . 2000;73:552–557
  37. Chae HD , Kim CH , Kang BM , Chang YS . Clinical usefulness of basal FSH as a prognostic factor in patients undergoing intracytoplasmic sperm injection . J Obstet Gynaecol Res . 2000;26:55–60
  38. Chuang CC , Chen CD , Chao KH , Chen SU , Ho HN , Yang YS . Age is a better predictor of pregnancy potential than basal follicle-stimulating hormone levels in women undergoing in vitro fertilization . Fertil Steril . 2003;79:63–68
  39. Creus M , Penarrubia J , Fabregues F , Vidal E , Carmona F , Casamitjana R , et al.  Day 3 serum inhibin B and FSH and age as predictors of assisted reproduction treatment outcome . Hum Reprod . 2000;15:2341–2346
  40. Fabregues F , Balasch J , Creus M , Carmona F , Puerto B , Quinto L , et al.  Ovarian reserve test with human menopausal gonadotropin as a predictor of in vitro fertilization outcome . J Assist Reprod Genet . 2000;17:13–19
  41. Jinno M , Hoshiai T , Nakamura Y , Teruya K , Tsunoda T . A novel method for assessing assisted female fertility: bioelectric impedance . J Clin Endocrinol Metab . 2000;85:471–474
  42. Mikkelsen AL , Andersson AM , Skakkebaek NE , Lindenberg S . Basal concentrations of oestradiol may predict the outcome of in-vitro maturation in regularly menstruating women . Hum Reprod . 2001;16:862–867
  43. Penarrubia J , Balasch J , Fabregues F , Carmona F , Casamitjana R , Moreno V , et al.  Day 5 inhibin B serum concentrations as predictors of assisted reproductive technology outcome in cycles stimulated with gonadotrophin-releasing hormone agonist-gonadotrophin treatment . Hum Reprod . 2000;15:1499–1504
  44. van der Stege JG , van der Linden PJ . Useful predictors of ovarian stimulation response in women undergoing in vitro fertilization . Gynecol Obstet Invest . 2001;52:43–46
  45. Yanushpolsky EH , Hurwitz S , Tikh E , Racowsky C . Predictive usefulness of cycle day 10 follicle-stimulating hormone level in a clomiphene citrate challenge test for in vitro fertilization outcome in women younger than 40 years of age . Fertil Steril . 2003;80:111–115
  46. Templeton A , Morris JK , Parslow W . Factors that affect outcome of in-vitro fertilisation treatment . Lancet . 1996;348:1402–1406
  47. Scott RT , Toner JP , Muasher SJ , Oehninger S , Robinson S , Rosenwaks Z . Follicle-stimulating hormone levels on cycle day 3 are predictive of in vitro fertilization outcome . Fertil Steril . 1989;51:651–654
  48. Barnhart K , Osheroff J . Follicle stimulating hormone as a predictor of fertility . Curr Opin Obstet Gynecol . 1998;10:227–232
  49. Scott RT , Hofmann GE , Oehninger S , Muasher SJ . Intercycle variability of day 3 follicle-stimulating hormone levels and its effect on stimulation quality in in vitro fertilization . Fertil Steril . 1990;54:297–302
  50. Bancsi LF , Broekmans FJ , Looman CW , Habbema JD , te Velde ER . Predicting poor ovarian response in IVF: use of repeat basal FSH measurement . J Reprod Med . 2004;49:187–194
  51. Sharara FI , Scott RT , Seifer DB . The detection of diminished ovarian reserve in infertile women . Am J Obstet Gynecol . 1998;179:804–812
  52. van Rooij IA , Bancsi LF , Broekmans FJ , Looman CW , Habbema JD , te Velde ER . Women older than 40 years of age and those with elevated follicle-stimulating hormone levels differ in poor response rate and embryo quality in in vitro fertilization . Fertil Steril . 2003;79:482–488
  53. Schipper I , de Jong FH , Fauser BC . Lack of correlation between maximum early follicular phase serum follicle stimulating hormone concentrations and menstrual cycle characteristics in women under the age of 35 years . Hum Reprod . 1998;13:1442–1448
  54. Lambalk CB , Boomsma DI , De Boer L , De Koning CH , Schoute E , Popp-Snijders C , et al.  Increased levels and pulsatility of follicle-stimulating hormone in mothers of hereditary dizygotic twins . J Clin Endocrinol Metab . 1998;83:481–486
  55. Perez MM , Gromoll J , Behre HM , Gassner C , Nieschlag E , Simoni M . Ovarian response to follicle-stimulating hormone (FSH) stimulation depends on the FSH receptor genotype . J Clin Endocrinol Metab . 2000;85:3365–3369
  56. Sudo S , Kudo M , Wada S , Sato O , Hsueh AJ , Fujimoto S . Genetic and functional analyses of polymorphisms in the human FSH receptor gene . Mol Hum Reprod . 2002;8:893–899
  57. Hansen KR , Morris JL , Thyer AC , Soules MR . Reproductive aging and variability in the ovarian antral follicle count: application in the clinical setting . Fertil Steril . 2003;80:577–583
  58. Bancsi LF , Broekmans FJ , Looman CW , Habbema JD , te Velde ER . 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
  59. Kwee J , Schats R , McDonnell J , Lambalk CB , Schoemaker J . Intercycle variability of ovarian reserve tests: results of a prospective randomized study . Hum Reprod . 2004;19:590–595
  60. Klinkert ER , Broekmans FJ , Looman CW , te Velde ER . 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

PII: S0015-0282(04)02840-7

doi: 10.1016/j.fertnstert.2004.10.011

Fertility and Sterility
Volume 83, Issue 2 , Pages 291-301 , February 2005