Skip to main content
SpringerLink
Log in

Effects of malignancies on fertility preservation outcomes and relevant cryobiological advances

  • Review
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

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.

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

Similar content being viewed by others

References

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Baerwald, A.R., Adams, G.P., and Pierson, R.A. (2003a). Characterization of ovarian follicular wave dynamics in women. Biol Reprod 69, 1023–1031.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Balasch, J., and Gratacós, E. (2011). Delayed childbearing: effects on fertility and the outcome of pregnancy. Fetal Diagn Ther 29, 263–273.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bornstein, S.R., Rutkowski, H., and Vrezas, I. (2004). Cytokines and steroidogenesis. Mol Cell Endocrinol 215, 135–141.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Brenner, B., Avivi, I., and Lishner, M. (2012). Haematological cancers in pregnancy. Lancet 379, 580–587.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Cakmak, H., and Rosen, M.P. (2013). Ovarian stimulation in cancer patients. Fertil Steril 99, 1476–1484.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Donnez, J., and Dolmans, M.M. (2017). Fertility preservation in women. N Engl J Med 377, 1657–1665.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Book  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gougeon, A. (1986). Dynamics of follicular growth in the human: a model from preliminary results. Hum Reprod 1, 81–87.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Jemal, A., Siegel, R., Xu, J., and Ward, E. (2010). Cancer statistics, 2010. CA Cancer J Clin 60, 277–300.

    Article  PubMed  Google Scholar 

  • Kaplan, J.R., and Manuck, S.B. (2004). Ovarian dysfunction, stress, and disease: a primate continuum. ILAR J 45, 89–115.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Offit, K., Sagi, M., and Hurley, K. (2006). Preimplantation genetic diagnosis for cancer syndromes. JAMA 296, 2727–2730.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pacheco, F., and Oktay, K. (2017). Current success and efficiency of autologous ovarian transplantation: a meta-analysis. Reprod Sci 24, 1111–1120.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Visvader, J.E. (2011). Cells of origin in cancer. Nature 469, 314–322.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Walls, M.L., and Hart, R.J. (2018). In vitro maturation. Best Pract Res Clin Obstet Gynaecol 53, 60–72.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yip, C.H., and Rhodes, A. (2014). Estrogen and progesterone receptors in breast cancer. Future Oncol 10, 2293–2301.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

  1. Reproductive Medical Center, Department of Obstetrics and Gynecology, Peking University Third Hospital, Beijing, 100191, China

    Dongming Liu, Jie Yan & Jie Qiao

  2. National Clinical Center for Obstetrics and Gynecology, Beijing, 100191, China

    Dongming Liu, Jie Yan & Jie Qiao

  3. Key Laboratory of Assisted Reproduction, Ministry of Education, Beijing, 100191, China

    Dongming Liu, Jie Yan & Jie Qiao

  4. Beijing Key Laboratory of Reproductive Endocrinology and Assisted Reproduction, Beijing, 100191, China

    Dongming Liu, Jie Yan & Jie Qiao

Authors
  1. Dongming Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jie Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jie Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jie Yan.

Ethics declarations

The author(s) declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, D., Yan, J. & Qiao, J. Effects of malignancies on fertility preservation outcomes and relevant cryobiological advances. Sci. China Life Sci. 63, 217–227 (2020). https://doi.org/10.1007/s11427-019-9526-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-019-9526-2

Keywords

Search

Navigation