Effects of malignancies on fertility preservation outcomes and relevant cryobiological advances

  • Dongming Liu
  • Jie YanEmail author
  • Jie Qiao


A decrease in cancer deaths has resulted in the possibility of child bearing for many young adult cancer survivors. Most antitumor treatment modalities are detrimental to female fertility, and methods for fertility preservation before gonadotoxic treatment, including cryopreservation of oocytes, embryos and ovarian tissue, have therefore been developed. This review focuses on the ovarian function of cancer patients, the safety and efficacy of fertility preservation methods, and the pregnancy outcomes of these patients. Breast cancer and hematological tumors constitute the majority of cancers in reproductive-aged female oncology patients. Ovarian function may not be impacted by breast cancer cells, while in patients with hematological malignancies, decreases in anti-Müllerian hormone and antral follicle counts have been demonstrated. In most cases, patients can undergo ovarian stimulation without delaying treatment, and a new stimulation protocol known as dual stimulation, which may be more efficient, has now been developed. Birth outcomes are also acceptable in cancer patients.


cancer patients fertility preservation controlled ovarian stimulation safety 


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This work was supported by the National Key Technology R&D Program of China (2017YFC1002004, 2018YFC1004001) and National Natural Science Foundation of China (81571386, 81730038, 31429004).


  1. Allen, P.B., Pavone, M.E., Smith, K.N., Kazer, R.R., Rademaker, A., Lawson, A.K., Moravek, M.B., Confino, R., Gordon, L.I., and Winter, J.N. (2018). The impact of fertility preservation on treatment delay and progression-free survival in women with lymphoma: a single-centre experience. Br J Haematol 180, 901–904.CrossRefPubMedGoogle Scholar
  2. Almog, B., Azem, F., Gordon, D., Pauzner, D., Amit, A., Barkan, G., and Levin, I. (2012). Effects of cancer on ovarian response in controlled ovarian stimulation for fertility preservation. Fertil Steril 98, 957–960.CrossRefPubMedGoogle Scholar
  3. Alvarez, R.M., and Ramanathan, P. (2018). Fertility preservation in female oncology patients: the influence of the type of cancer on ovarian stimulation response. Hum Reprod 33, 2051–2059.PubMedGoogle Scholar
  4. Anderson, C., Engel, S.M., Mersereau, J.E., Black, K.Z., Wood, W.A., Anders, C.K., and Nichols, H.B. (2017). Birth outcomes among adolescent and young adult cancer survivors. JAMA Oncol 3, 1078–1084.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Antoniou, A., Pharoah, P.D.P., Narod, S., Risch, H.A., Eyfjord, J.E., Hopper, J.L., Loman, N., Olsson, H., Johannsson, O., Borg, A., et al. (2003). Average risks of breast and ovarian cancer associated with BRCA1 or BRCA2 mutations detected in case Series unselected for family history: a combined analysis of 22 studies. Am J Human Genet 72, 1117–1130.CrossRefGoogle Scholar
  6. Armuand, G.M., Wettergren, L., Rodriguez-Wallberg, K.A., and Lampic, C. (2014). Desire for children, difficulties achieving a pregnancy, and infertility distress 3 to 7 years after cancer diagnosis. Supp Care Cancer 22, 2805–2812.CrossRefGoogle Scholar
  7. Baerwald, A.R., Adams, G.P., and Pierson, R.A. (2003a). Characterization of ovarian follicular wave dynamics in women. Biol Reprod 69, 1023–1031.CrossRefPubMedGoogle Scholar
  8. Baerwald, A.R., Adams, G.P., and Pierson, R.A. (2003b). A new model for ovarian follicular development during the human menstrual cycle. Fertil Steril 80, 116–122.CrossRefPubMedGoogle Scholar
  9. Balasch, J., and Gratacós, E. (2011). Delayed childbearing: effects on fertility and the outcome of pregnancy. Fetal Diagn Ther 29, 263–273.CrossRefPubMedGoogle Scholar
  10. Baynosa, J., Westphal, L.M., Madrigrano, A., and Wapnir, I. (2009). Timing of breast cancer treatments with oocyte retrieval and embryo cryopreservation. J Am Coll Surg 209, 603–607.CrossRefPubMedGoogle Scholar
  11. Boots, C.E., Meister, M., Cooper, A.R., Hardi, A., and Jungheim, E.S. (2016). Ovarian stimulation in the luteal phase: systematic review and meta-analysis. J Assist Reprod Genet 33, 971–980.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bornstein, S.R., Rutkowski, H., and Vrezas, I. (2004). Cytokines and steroidogenesis. Mol Cell Endocrinol 215, 135–141.CrossRefPubMedGoogle Scholar
  13. Bray, F., Ferlay, J., Soerjomataram, I., Siegel, R.L., Torre, L.A., and Jemal, A. (2018). Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68, 394–424.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Brenner, B., Avivi, I., and Lishner, M. (2012). Haematological cancers in pregnancy. Lancet 379, 580–587.CrossRefPubMedGoogle Scholar
  15. Cakmak, H., Katz, A., Cedars, M.I., and Rosen, M.P. (2013). Effective method for emergency fertility preservation: random-start controlled ovarian stimulation. Fertil Steril 100, 1673–1680.CrossRefPubMedGoogle Scholar
  16. Cakmak, H., and Rosen, M.P. (2013). Ovarian stimulation in cancer patients. Fertil Steril 99, 1476–1484.CrossRefPubMedGoogle Scholar
  17. Cardozo, E.R., Thomson, A.P., Karmon, A.E., Dickinson, K.A., Wright, D. L., and Sabatini, M.E. (2015). Ovarian stimulation and in-vitro fertilization outcomes of cancer patients undergoing fertility preservation compared to age matched controls: a 17-year experience. J Assist Reprod Genet 32, 587–596.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Chan, J.L., Johnson, L.N.C., Efymow, B.L., Sammel, M.D., and Gracia, C. R. (2015). Outcomes of ovarian stimulation after treatment with chemotherapy. J Assist Reprod Genet 32, 1537–1545.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Checa, M.A., Brassesco, M., Sastre, M., Gómez, M., Herrero, J., Marque, L., Brassesco, A., and Espinós, J.J. (2015). Random-start GnRH antagonist for emergency fertility preservation: a self-controlled trial. Int J Womens Health 7, 219–225.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Checa Vizcaíno, M.A., Corchado, A.R., Sastre I. Cuadri, M.E., Comadran, M.G., Brassesco, M., and Carreras, R. (2012). The effects of letrozole on ovarian stimulation for fertility preservation in cancer-affected women. Reprod Biomed Online 24, 606–610.CrossRefPubMedGoogle Scholar
  21. Chien, A.J., Chambers, J., Mcauley, F., Kaplan, T., Letourneau, J., Hwang, J., Kim, M.O., Melisko, M.E., Rugo, H.S., Esserman, L.J., et al. (2017). Fertility preservation with ovarian stimulation and time to treatment in women with stage II-III breast cancer receiving neoadjuvant therapy. Breast Cancer Res Treat 165, 151–159.CrossRefPubMedGoogle Scholar
  22. Cobo, A., García- Velasco, J., Domingo, J., Pellicer, A., and Remohí, J. (2018). Elective and onco-fertility preservation: factors related to IVF outcomes. Hum Reprod 33, 2222–2231.CrossRefPubMedGoogle Scholar
  23. Cobo, A., Serra, V., Garrido, N., Olmo, I., Pellicer, A., and Remohí, J. (2014). Obstetric and perinatal outcome of babies born from vitrified oocytes. Fertil Steril 102, 1006–1015.e4.CrossRefPubMedGoogle Scholar
  24. Codacci-Pisanelli, G., Del Pup, L., Del Grande, M., and Peccatori, F.A. (2017). Mechanisms of chemotherapy-induced ovarian damage in breast cancer patients. Crit Rev Oncol/Hematol 113, 90–96.CrossRefGoogle Scholar
  25. Creux, H., Monnier, P., Son, W.Y., and Buckett, W. (2018). Thirteen years' experience in fertility preservation for cancer patients after in vitro fertilization and in vitro maturation treatments. J Assist Reprod Genet 35, 583–592.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Decanter, C., Robin, G., Mailliez, A., Sigala, J., Morschhauser, F., Ramdane, N., Devos, P., Dewailly, D., Leroy-Martin, B., and Keller, L. (2018). Prospective assessment of follicular growth and the oocyte cohort after ovarian stimulation for fertility preservation in 90 cancer patients versus 180 matched controls. Reprod Biomed Online 36, 543–551.CrossRefPubMedGoogle Scholar
  27. Demeestere, I., Brice, P., Peccatori, F.A., Kentos, A., Dupuis, J., Zachee, P., Casasnovas, O., Van Den Neste, E., Dechene, J., De Maertelaer, V., et al. (2016). No evidence for the benefit of gonadotropin-releasing hormone agonist in preserving ovarian function and fertility in lymphoma survivors treated with chemotherapy: final long-term report of a prospective randomized trial. J Clin Oncol 34, 2568–2574.CrossRefPubMedGoogle Scholar
  28. Derks-Smeets, I.A.P., van Tilborg, T.C., van Montfoort, A., Smits, L., Torrance, H.L., Meijer-Hoogeveen, M., Broekmans, F., Dreesen, J.C.F. M., Paulussen, A.D.C., Tjan-Heijnen, V.C.G., et al. (2017). BRCA1 mutation carriers have a lower number of mature oocytes after ovarian stimulation for IVF/PGD. J Assist Reprod Genet 34, 1475–1482.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Deura, I., Harada, T., Taniguchi, F., Iwabe, T., Izawa, M., and Terakawa, N. (2005). Reduction of estrogen production by interleukin-6 in a human granulosa tumor cell line may have implications for endometriosis-associated infertility. Fertil Steril 83, 1086–1092.CrossRefPubMedGoogle Scholar
  30. Dolmans, M.M., Luyckx, V., Donnez, J., Andersen, C.Y., and Greve, T. (2013). Risk of transferring malignant cells with transplanted frozen-thawed ovarian tissue. Fertil Steril 99, 1514–1522.CrossRefPubMedGoogle Scholar
  31. Domingo, J., Guillén, V., Ayllón, Y., Martínez, M., Muñoz, E., Pellicer, A., and Garcia-Velasco, J.A. (2012). Ovarian response to controlled ovarian hyperstimulation in cancer patients is diminished even before oncological treatment. Fertil Steril 97, 930–934.CrossRefPubMedGoogle Scholar
  32. Donnez, J., and Dolmans, M.M. (2017). Fertility preservation in women. N Engl J Med 377, 1657–1665.CrossRefPubMedGoogle Scholar
  33. Drakopoulos, P., Blockeel, C., Stoop, D., Camus, M., de Vos, M., Tournaye, H., and Polyzos, N.P. (2016). Conventional ovarian stimulation and single embryo transfer for IVF/ICSI. How many oocytes do we need to maximize cumulative live birth rates after utilization of all fresh and frozen embryos? Hum Reprod 31, 370–376.Google Scholar
  34. Druckenmiller, S., Goldman, K.N., Labella, P.A., Fino, M.E., Bazzocchi, A., and Noyes, N. (2016). Successful oocyte cryopreservation in reproductive-aged cancer survivors. Obstetr Gynecol 127, 474–480.CrossRefGoogle Scholar
  35. Fabbri, R., Pasquinelli, G., Magnani, V., Arpinati, M., Battaglia, C., Paradisi, R., and Venturoli, S. (2011). Follicle features in adolescent and young adult women with Hodgkin's disease prior to chemotherapy: a preliminary report. Reprod Biomed Online 23, 799–805.CrossRefPubMedGoogle Scholar
  36. Fossa, S.D., Magelssen, H., Melve, K., Jacobsen, A.B., Langmark, F., and Skjaerven, R. (2005). Parenthood in survivors after adulthood cancer and perinatal health in their offspring: a preliminary report. J Natl Cancer Inst Monogr 77–82.Google Scholar
  37. Friedler, S., Koc, O., Gidoni, Y., Raziel, A., and Ron-El, R. (2012). Ovarian response to stimulation for fertility preservation in women with malignant disease: a systematic review and meta-analysis. Fertil Steril 97, 125–133.CrossRefPubMedGoogle Scholar
  38. Gagliato, D.M., Gonzalez-Angulo, A.M., Lei, X., Theriault, R.L., Giordano, S.H., Valero, V., Hortobagyi, G.N., and Chavez-Macgregor, M. (2014). Clinical impact of delaying initiation of adjuvant chemotherapy in patients with breast cancer. J Clin Oncol 32, 735–744.CrossRefPubMedCentralGoogle Scholar
  39. Gietel-Habets, J.J.G., de Die-Smulders, C.E.M., Tjan-Heijnen, V.C.G., Derks-Smeets, I.A.P., van Golde, R., Gomez-Garcia, E., and van Osch, L.A.D.M. (2018). Professionals' knowledge, attitude and referral behaviour of preimplantation genetic diagnosis for hereditary breast and ovarian cancer. Reprod Biomed Online 36, 137–144.CrossRefPubMedGoogle Scholar
  40. Ginther, O.J., Beg, M.A., Gastal, E.L., Gastal, M.O., Baerwald, A.R., and Pierson, R.A. (2005). Systemic concentrations of hormones during the development of follicular waves in mares and women: a comparative study. Reproduction 130, 379–388.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Glujovsky, D., Riestra, B., Sueldo, C., Fiszbajn, G., Repping, S., Nodar, F., Papier, S., and Ciapponi, A. (2014). Vitrification versus slow freezing for women undergoing oocyte cryopreservation. Cochrane Database Syst Rev CD010047.CrossRefGoogle Scholar
  42. Gorman, J.R., Malcarne, V.L., Roesch, S.C., Madlensky, L., and Pierce, J.P. (2010). Depressive symptoms among young breast cancer survivors: the importance of reproductive concerns. Breast Cancer Res Treat 123, 477–485.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Gougeon, A. (1986). Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod 1, 81–87.CrossRefPubMedGoogle Scholar
  44. Guzman, R.C., Yang, J., Rajkumar, L., Thordarson, G., Chen, X., and Nandi, S. (1999). Hormonal prevention of breast cancer: mimicking the protective effect of pregnancy. Proc Natl Acad Sci USA 96, 2520–2525.CrossRefPubMedGoogle Scholar
  45. Haggar, F.A., Pereira, G., Preen, D., Holman, C.D.A., and Einarsdottir, K. (2014). Adverse obstetric and perinatal outcomes following treatment of adolescent and young adult cancer: a population-based cohort study. PLoS ONE 9, e113292.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Hammarberg, K., Kirkman, M., Stern, C., McLachlan, R.I., Clarke, G., Agresta, F., Gook, D., Rombauts, L., Vollenhoven, B., and Fisher, J.R. W. (2017). Survey of reproductive experiences and outcomes of cancer survivors who stored reproductive material before treatment. Hum Reprod 32, 2423–2430.CrossRefPubMedGoogle Scholar
  47. Hartman, E.K., and Eslick, G.D. (2016). The prognosis of women diagnosed with breast cancer before, during and after pregnancy: a meta-analysis. Breast Cancer Res Treat 160, 347–360.CrossRefPubMedGoogle Scholar
  48. Hulsbosch, S., Koskas, M., Tomassetti, C., De Sutter, P., Wildiers, H., Neven, P., D'Hooghe, T., and Amant, F. (2018). A real-life analysis of reproductive outcome after fertility preservation in female cancer patients. Gynecol Obstet Invest 83, 156–163.CrossRefPubMedGoogle Scholar
  49. Huyghe, E., Sui, D., Odensky, E., and Schover, L.R. (2009). Needs assessment survey to justify establishing a reproductive health clinic at a comprehensive cancer center. J Sex Med 6, 149–163.CrossRefPubMedGoogle Scholar
  50. Jemal, A., Siegel, R., Xu, J., and Ward, E. (2010). Cancer statistics, 2010. CA Cancer J Clin 60, 277–300.CrossRefPubMedGoogle Scholar
  51. Kaplan, J.R., and Manuck, S.B. (2004). Ovarian dysfunction, stress, and disease: a primate continuum. ILAR J 45, 89–115.CrossRefPubMedGoogle Scholar
  52. Kedem, A., Yerushalmi, G.M., Brengauz, M., Raanani, H., Orvieto, R., Hourvitz, A., and Meirow, D. (2018). Outcome of immature oocytes collection of 119 cancer patients during ovarian tissue harvesting for fertility preservation. J Assist Reprod Genet 35, 851–856.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kim, J.H., Kim, S.K., Lee, H.J., Lee, J.R., Jee, B.C., Suh, C.S., and Kim, S. H. (2015). Efficacy of random-start controlled ovarian stimulation in cancer patients. J Korean Med Sci 30, 290–295.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Kimler, B.F., Briley, S.M., Johnson, B.W., Armstrong, A.G., Jasti, S., and Duncan, F.E. (2018). Radiation-induced ovarian follicle loss occurs without overt stromal changes. Reproduction 155, 553–562.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Klock, S.C., Zhang, J.X., and Kazer, R.R. (2010). Fertility preservation for female cancer patients: early clinical experience. Fertil Steril 94, 149–155.CrossRefPubMedGoogle Scholar
  56. Knopman, J.M., Noyes, N., Talebian, S., Krey, L.C., Grifo, J.A., and Licciardi, F. (2009). Women with cancer undergoing ART for fertility preservation: a cohort study of their response to exogenous gonadotropins. Fertil Steril 91, 1476–1478.CrossRefPubMedGoogle Scholar
  57. Kuang, Y., Chen, Q., Hong, Q., Lyu, Q., Ai, A., Fu, Y., and Shoham, Z. (2014). Double stimulations during the follicular and luteal phases of poor responders in IVF/ICSI programmes (Shanghai protocol). Reprod Biomed Online 29, 684–691.CrossRefPubMedGoogle Scholar
  58. Kuang, Y., Hong, Q., Chen, Q., Lyu, Q., Ai, A., Fu, Y., and Shoham, Z. (2014). Luteal-phase ovarian stimulation is feasible for producing competent oocytes in women undergoing in vitro fertilization/ intracytoplasmic sperm injection treatment, with optimal pregnancy outcomes in frozen-thawed embryo transfer cycles. Fertil Steril 101, 105–111.CrossRefPubMedGoogle Scholar
  59. Laronda, M.M., Rutz, A.L., Xiao, S., Whelan, K.A., Duncan, F.E., Roth, E. W., Woodruff, T.K., and Shah, R.N. (2017). A bioprosthetic ovary created using 3D printed microporous scaffolds restores ovarian function in sterilized mice. Nat Commun 8, 15261.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Lawrenz, B., Fehm, T., von Wolff, M., Soekler, M., Huebner, S., Henes, J., Henes, M., and Henes, M. (2012). Reduced pretreatment ovarian reserve in premenopausal female patients with Hodgkin lymphoma or non-Hodgkin-lymphoma—evaluation by using antimüllerian hormone and retrieved oocytes. Fertil Steril 98, 141–144.CrossRefPubMedGoogle Scholar
  61. Lekovich, J., Lobel, A.L.S., Stewart, J.D., Pereira, N., Kligman, I., and Rosenwaks, Z. (2016). Female patients with lymphoma demonstrate diminished ovarian reserve even before initiation of chemotherapy when compared with healthy controls and patients with other malignancies. J Assist Reprod Genet 33, 657–662.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Leonard, R.C.F., Adamson, D.J.A., Bertelli, G., Mansi, J., Yellowlees, A., Dunlop, J., Thomas, G.A., Coleman, R.E., and Anderson, R.A. (2017). GnRH agonist for protection against ovarian toxicity during chemotherapy for early breast cancer: the Anglo Celtic Group OPTION trial. Ann Oncol 28, 1811–1816.CrossRefPubMedGoogle Scholar
  63. Letourneau, J.M., Sinha, N., Wald, K., Harris, E., Quinn, M., Imbar, T., Mok- Lin, E., Chien, A.J., and Rosen, M. (2017). Random start ovarian stimulation for fertility preservation appears unlikely to delay initiation of neoadjuvant chemotherapy for breast cancer. Hum Reprod 32, 2123–2129.CrossRefPubMedGoogle Scholar
  64. Li, G., Guo, X., Tang, L., Chen, M., Luo, X., Peng, L., Xu, X., Wang, S., Xiao, Z., Yi, W., et al. (2017). Analysis of BRCA1/2 mutation spectrum and prevalence in unselected Chinese breast cancer patients by next-generation sequencing. J Cancer Res Clin Oncol 143, 2011–2024.CrossRefPubMedGoogle Scholar
  65. Liang, Y., Fu, X.W., Li, J.J., Yuan, D.S., and Zhu, S.E. (2014). DNA methylation pattern in mouse oocytes and their in vitro fertilized early embryos: effect of oocyte vitrification. Zygote 22, 138–145.CrossRefPubMedGoogle Scholar
  66. Liu, C., Jiang, H., Zhang, W., and Yin, H. (2017). Double ovarian stimulation during the follicular and luteal phase in women ≥38 years: a retrospective case-control study. Reprod Biomed Online 35, 678–684.CrossRefPubMedGoogle Scholar
  67. Luyckx, V., Dolmans, M.M., Vanacker, J., Legat, C., Fortuño Moya, C., Donnez, J., and Amorim, C.A. (2014). A new step toward the artificial ovary: survival and proliferation of isolated murine follicles after autologous transplantation in a fibrin scaffold. Fertil Steril 101, 1149–1156.CrossRefPubMedGoogle Scholar
  68. Martinez, F., Clua, E., Devesa, M., Rodríguez, I., Arroyo, G., González, C., Solé, M., Tur, R., Coroleu, B., and Barri, P.N. (2014). Comparison of starting ovarian stimulation on day 2 versus day 15 of the menstrual cycle in the same oocyte donor and pregnancy rates among the corresponding recipients of vitrified oocytes. Fertil Steril 102, 1307–1311.CrossRefPubMedGoogle Scholar
  69. Martinez, M., Rabadan, S., Domingo, J., Cobo, A., Pellicer, A., and Garcia-Velasco, J.A. (2014). Obstetric outcome after oocyte vitrification and warming for fertility preservation in women with cancer. Reprod Biomed Online 29, 722–728.CrossRefPubMedGoogle Scholar
  70. Merker, V.L., Murphy, T.P., Hughes, J.B., Muzikansky, A., Hughes, M.R., Souter, I., and Plotkin, S.R. (2015). Outcomes of preimplantation genetic diagnosis in neurofibromatosis type 1. Fertil Steril 103, 761–768.e1.CrossRefPubMedGoogle Scholar
  71. Michaan, N., Ben-David, G., Ben-Yosef, D., Almog, B., Many, A., Pauzner, D., Lessing, J.B., Amit, A., and Azem, F. (2010). Ovarian stimulation and emergency in vitro fertilization for fertility preservation in cancer patients. Eur J Obstet Gynecol Reprod Biol 149, 175–177.CrossRefPubMedGoogle Scholar
  72. Moore, H.C.F., Unger, J.M., Phillips, K.A., Boyle, F., Hitre, E., Porter, D., Francis, P.A., Goldstein, L.J., Gomez, H.L., Vallejos, C.S., et al. (2015). Goserelin for ovarian protection during breast-cancer adjuvant chemotherapy. N Engl J Med 372, 923–932.CrossRefPubMedPubMedCentralGoogle Scholar
  73. Offit, K., Sagi, M., and Hurley, K. (2006). Preimplantation genetic diagnosis for cancer syndromes. JAMA 296, 2727–2730.CrossRefPubMedGoogle Scholar
  74. Oktay, K., Harvey, B.E., Partridge, A.H., Quinn, G.P., Reinecke, J., Taylor, H.S., Wallace, W.H., Wang, E.T., and Loren, A.W. (2018). Fertility preservation in patients with cancer: ASCO clinical practice guideline update. J Clin Oncol 36, 1994–2001.CrossRefPubMedGoogle Scholar
  75. Oktay, K., Hourvitz, A., Sahin, G., Oktem, O., Safro, B., Cil, A., and Bang, H. (2006). Letrozole reduces estrogen and gonadotropin exposure in women with breast cancer undergoing ovarian stimulation before chemotherapy. J Clin Endocrinol Metab 91, 3885–3890.CrossRefPubMedGoogle Scholar
  76. Oktay, K., Turan, V., Bedoschi, G., Pacheco, F.S., and Moy, F. (2015). Fertility preservation success subsequent to concurrent aromatase inhibitor treatment and ovarian stimulation in women with breast cancer. J Clin Oncol 33, 2424–2429.CrossRefPubMedPubMedCentralGoogle Scholar
  77. Pacheco, F., and Oktay, K. (2017). Current success and efficiency of autologous ovarian transplantation: a meta-analysis. Reprod Sci 24, 1111–1120.CrossRefPubMedGoogle Scholar
  78. Pal, L., Leykin, L., Schifren, J.L., Isaacson, K.B., Chang, Y.C., Nikruil, N., Chen, Z., and Toth, T.L. (1998). Malignancy may adversely influence the quality and behaviour of oocytes. Hum Reprod 13, 1837–1840.CrossRefPubMedGoogle Scholar
  79. Paradisi, R., Vicenti, R., Macciocca, M., Seracchioli, R., Rossi, S., and Fabbri, R. (2016). High cytokine expression and reduced ovarian reserve in patients with Hodgkin lymphoma or non-Hodgkin lymphoma. Fertil Steril 106, 1176–1182.CrossRefPubMedGoogle Scholar
  80. Paulini, F., Vilela, J.M.V., Chiti, M.C., Donnez, J., Jadoul, P., Dolmans, M. M., and Amorim, C.A. (2016). Survival and growth of human preantral follicles after cryopreservation of ovarian tissue, follicle isolation and short-term xenografting. Reprod Biomed Online 33, 425–432.CrossRefPubMedGoogle Scholar
  81. Pinnix, C.C., Osborne, E.M., Chihara, D., Lai, P., Zhou, S., Ramirez, M.M., Oki, Y., Hagemeister, F.B., Rodriguez, A.M., Samaniego, F., et al. (2016). Maternal and fetal outcomes after therapy for Hodgkin or non-Hodgkin lymphoma diagnosed during pregnancy. JAMA Oncol 2, 1065–1069.CrossRefPubMedGoogle Scholar
  82. Platet, N., Cathiard, A.M., Gleizes, M., and Garcia, M. (2004). Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. Crit Rev Oncol/Hematol 51, 55–67.CrossRefGoogle Scholar
  83. Quinn, G.P., Block, R.G., Clayman, M.L., Kelvin, J., Arvey, S.R., Lee, J.H., Reinecke, J., Sehovic, I., Jacobsen, P.B., Reed, D., et al. (2015). If you did not document it, it did not happen: rates of documentation of discussion of infertility risk in adolescent and young adult oncology patients' medical records. J Oncol Pract 11, 137–144.CrossRefPubMedGoogle Scholar
  84. Quinn, M.M., Cakmak, H., Letourneau, J.M., Cedars, M.I., and Rosen, M. P. (2017). Response to ovarian stimulation is not impacted by a breast cancer diagnosis. Hum Reprod 32, 568–574.PubMedGoogle Scholar
  85. Quintero, R.B., Helmer, A., Huang, J.Q., and Westphal, L.M. (2010). Ovarian stimulation for fertility preservation in patients with cancer. Fertil Steril 93, 865–868.CrossRefPubMedGoogle Scholar
  86. Rapoport, B.L., Demetriou, G.S., Moodley, S.D., and Benn, C.A. (2014). When and how do I use neoadjuvant chemotherapy for breast cancer? Curr Treat Options Oncol 15, 86–98.CrossRefPubMedGoogle Scholar
  87. Revelli, A., Porcu, E., Levi Setti, P.E., Delle Piane, L., Merlo, D.F., and Anserini, P. (2013). Is letrozole needed for controlled ovarian stimulation in patients with estrogen receptor-positive breast cancer? Gynecol Endocrinol 29, 993–996.CrossRefPubMedGoogle Scholar
  88. Robertson, A.D., Missmer, S.A., and Ginsburg, E.S. (2011). Embryo yield after in vitro fertilization in women undergoing embryo banking for fertility preservation before chemotherapy. Fertil Steril 95, 588–591.CrossRefPubMedGoogle Scholar
  89. Rodgers, R.J., Reid, G.D., Koch, J., Deans, R., Ledger, W.L., Friedlander, M., Gilchrist, R.B., Walters, K.A., and Abbott, J.A. (2017). The safety and efficacy of controlled ovarian hyperstimulation for fertility preservation in women with early breast cancer: a systematic review. Hum Reprod 32, 1033–1045.CrossRefPubMedGoogle Scholar
  90. Rosendahl, M., Greve, T., and Andersen, C.Y. (2013). The safety of transplanting cryopreserved ovarian tissue in cancer patients: a review of the literature. J Assist Reprod Genet 30, 11–24.CrossRefPubMedGoogle Scholar
  91. Samir, M., Glister, C., Mattar, D., Laird, M., and Knight, P.G. (2017). Follicular expression of pro-inflammatory cytokines tumour necrosis factor-α (TNFα), interleukin 6 (IL6) and their receptors in cattle: TNFα, IL6 and macrophages suppress thecal androgen production in vitro. Reproduction 154, 35–49.CrossRefPubMedGoogle Scholar
  92. Segers, I., Mateizel, I., Van Moer, E., Smitz, J., Tournaye, H., Verheyen, G., and De Vos, M. (2015). In vitro maturation (IVM) of oocytes recovered from ovariectomy specimens in the laboratory: a promising “ex vivo” method of oocyte cryopreservation resulting in the first report of an ongoing pregnancy in Europe. J Assist Reprod Genet 32, 1221–1231.CrossRefPubMedPubMedCentralGoogle Scholar
  93. Shapira, M., Raanani, H., Feldman, B., Srebnik, N., Dereck- Haim, S., Manela, D., Brenghausen, M., Geva- Lerner, L., Friedman, E., Levi-Lahad, E., et al. (2015). BRCA mutation carriers show normal ovarian response in in vitro fertilization cycles. Fertil Steril 104, 1162–1167.CrossRefPubMedGoogle Scholar
  94. Smith, G.D., Serafini, P.C., Fioravanti, J., Yadid, I., Coslovsky, M., Hassun, P., Alegretti, J.R., and Motta, E.L. (2010). Prospective randomized comparison of human oocyte cryopreservation with slow-rate freezing or vitrification. Fertil Steril 94, 2088–2095.CrossRefPubMedGoogle Scholar
  95. Smitz, J.E.J., Thompson, J.G., and Gilchrist, R.B. (2011). The promise of in vitro maturation in assisted reproduction and fertility preservation. Semin Reprod Med 29, 024–037.CrossRefGoogle Scholar
  96. Sonigo, C., Comtet, M., Duros, S., Sifer, C., Sermondade, N., and Grynberg, M. (2018). Antral follicle responsiveness to FSH, assessed by the follicular output rate (FORT), is altered in Hodgkin's lymphoma when compared with breast cancer candidates for fertility preservation. J Assist Reprod Genet 35, 91–97.CrossRefPubMedGoogle Scholar
  97. Stensheim, H., Klungsoyr, K., Skjaerven, R., Grotmol, T., and Fossa, S.D. (2013). Birth outcomes among offspring of adult cancer survivors: a population-based study. Int J Cancer 133, 2696–2705.PubMedGoogle Scholar
  98. Titus, S., Li, F., Stobezki, R., Akula, K., Unsal, E., Jeong, K., Dickler, M., Robson, M., Moy, F., Goswami, S., et al. (2013). Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans. Sci Transl Med 5, 172ra21.Google Scholar
  99. Toftager, M., Bogstad, J., Lossl, K., Praetorius, L., Zedeler, A., Bryndorf, T., Nilas, L., and Pinborg, A. (2017). Cumulative live birth rates after one ART cycle including all subsequent frozen-thaw cycles in 1050 women: secondary outcome of an RCT comparing GnRH-antagonist and GnRH-agonist protocols. Hum Reprod 32, 556–567.PubMedGoogle Scholar
  100. Torre, L.A., Islami, F., Siegel, R.L., Ward, E.M., and Jemal, A. (2017). Global cancer in women: burden and trends. Cancer Epidemiol Biomark Prev 26, 444–457.CrossRefGoogle Scholar
  101. Tsampras, N., Gould, D., and Fitzgerald, C.T. (2017). Double ovarian stimulation (DuoStim) protocol for fertility preservation in female oncology patients. Hum Fertil 20, 248–253.CrossRefGoogle Scholar
  102. Tsampras, N., Roberts, S.A., Gould, D., and Fitzgerald, C.T. (2018). Ovarian response to controlled ovarian stimulation for fertility preservation before oncology treatment: A retrospective cohort of 157 patients. Eur J Cancer Care 27, e12797.Google Scholar
  103. Turan, V., Bedoschi, G., Emirdar, V., Moy, F., and Oktay, K. (2018). Ovarian stimulation in patients with cancer: impact of letrozole and BRCA mutations on fertility preservation cycle outcomes. Reprod Sci 25, 26–32.CrossRefPubMedGoogle Scholar
  104. Ubaldi, F.M., Capalbo, A., Vaiarelli, A., Cimadomo, D., Colamaria, S., Alviggi, C., Trabucco, E., Venturella, R., Vajta, G., and Rienzi, L. (2016). Follicular versus luteal phase ovarian stimulation during the same menstrual cycle (DuoStim) in a reduced ovarian reserve population results in a similar euploid blastocyst formation rate: new insight in ovarian reserve exploitation. Fertil Steril 105, 1488–1495.e1.CrossRefPubMedGoogle Scholar
  105. Vaiarelli, A., Venturella, R., Vizziello, D., Bulletti, F., and Ubaldi, F.M. (2017). Dual ovarian stimulation and random start in assisted reproductive technologies. Curr Opin Obstet Gynecol 29, 153–159.CrossRefPubMedGoogle Scholar
  106. van Dorp, W., van den Heuvel-Eibrink, M.M., de Vries, A.C.H., Pluijm, S. M.F., Visser, J.A., Pieters, R., and Laven, J.S.E. (2014). Decreased serum anti-Mullerian hormone levels in girls with newly diagnosed cancer. Hum Reprod 29, 337–342.CrossRefPubMedGoogle Scholar
  107. Visvader, J.E. (2011). Cells of origin in cancer. Nature 469, 314–322.CrossRefPubMedGoogle Scholar
  108. von Wolff, M., Montag, M., Dittrich, R., Denschlag, D., Nawroth, F., and Lawrenz, B. (2011). Fertility preservation in women—a practical guide to preservation techniques and therapeutic strategies in breast cancer, Hodgkin's lymphoma and borderline ovarian tumours by the fertility preservation network FertiPROTEKT. Arch Gynecol Obstet 284, 427–435.CrossRefGoogle Scholar
  109. Wallace, W.H.B., Kelsey, T.W., and Anderson, R.A. (2016). Fertility preservation in pre-pubertal girls with cancer: the role of ovarian tissue cryopreservation. Fertil Steril 105, 6–12.CrossRefPubMedGoogle Scholar
  110. Wallace, W.H.B., Smith, A.G., Kelsey, T.W., Edgar, A.E., and Anderson, R. A. (2014). Fertility preservation for girls and young women with cancer: population-based validation of criteria for ovarian tissue cryopreservation. Lancet Oncol 15, 1129–1136.CrossRefPubMedPubMedCentralGoogle Scholar
  111. Walls, M.L., and Hart, R.J. (2018). In vitro maturation. Best Pract Res Clin Obstet Gynaecol 53, 60–72.CrossRefPubMedGoogle Scholar
  112. Wang, E.T., Pisarska, M.D., Bresee, C., Ida Chen, Y.D., Lester, J., Afshar, Y., Alexander, C., and Karlan, B.Y. (2014). BRCA1 germline mutations may be associated with reduced ovarian reserve. Fertil Steril 102, 1723- 1728.Google Scholar
  113. Wang, N., Li, C.Y., Zhu, H.B., Hao, H.S., Wang, H.Y., Yan, C.L., Zhao, S. J., Du, W.H., Wang, D., Liu, Y., et al. (2017). Effect of vitrification on the mRNA transcriptome of bovine oocytes. Reprod Dom Anim 52, 531–541.CrossRefGoogle Scholar
  114. Wang, N., Wang, Y., Chen, Q., Dong, J., Tian, H., Fu, Y., Ai, A., Lyu, Q., and Kuang, Y. (2016). Luteal-phase ovarian stimulation vs conventional ovarian stimulation in patients with normal ovarian reserve treated for IVF: a large retrospective cohort study. Clin Endocrinol 84, 720–728.CrossRefGoogle Scholar
  115. Winter, C., Nilsson, M.P., Olsson, E., George, A.M., Chen, Y., Kvist, A., Törngren, T., Vallon-Christersson, J., Hegardt, C., Häkkinen, J., et al. (2016). Targeted sequencing of BRCA1 and BRCA2 across a large unselected breast cancer cohort suggests that one-third of mutations are somatic. Ann Oncol 27, 1532–1538.CrossRefPubMedPubMedCentralGoogle Scholar
  116. Yasmin, E., Balachandren, N., Davies, M.C., Jones, G.L., Lane, S., Mathur, R., Webber, L., Anderson, R.A., and Anderson, R.A. (2018). Fertility preservation for medical reasons in girls and women: British fertility society policy and practice guideline. Hum Fertil 21, 3–26.CrossRefGoogle Scholar
  117. Yin, H., Jiang, H., Kristensen, S.G., and Andersen, C.Y. (2016). Vitrification of in vitro matured oocytes collected from surplus ovarian medulla tissue resulting from fertility preservation of ovarian cortex tissue. J Assist Reprod Genet 33, 741–746.CrossRefPubMedPubMedCentralGoogle Scholar
  118. Yip, C.H., and Rhodes, A. (2014). Estrogen and progesterone receptors in breast cancer. Future Oncol 10, 2293–2301.CrossRefPubMedGoogle Scholar
  119. Zhang, J., Sun, J., Chen, J., Yao, L., Ouyang, T., Li, J., Wang, T., Fan, Z., Fan, T., Lin, B., et al. (2016). Comprehensive analysis of BRCA1 and BRCA2 germline mutations in a large cohort of 5931 Chinese women with breast cancer. Breast Cancer Res Treat 158, 455–462.CrossRefPubMedGoogle Scholar
  120. Zhou, J., Huang, Y., Li, L., Zhu, L., Zhang, D., Zhang, S., and Chen, Y. (2013). Identification of two novel, alternatively spliced mRNA transcripts of the human follicle-stimulating hormone receptor. Mol Reprod Dev 80, 916–923.CrossRefPubMedGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Reproductive Medical Center, Department of Obstetrics and GynecologyPeking University Third HospitalBeijingChina
  2. 2.National Clinical Center for Obstetrics and GynecologyBeijingChina
  3. 3.Key Laboratory of Assisted ReproductionMinistry of EducationBeijingChina
  4. 4.Beijing Key Laboratory of Reproductive Endocrinology and Assisted ReproductionBeijingChina

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