Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 2/2019

01-02-2019 | Fertility Preservation

Chemotherapy-related damage to ovarian reserve in childhood cancer survivors: interpreting the evidence

Authors: Edgardo Somigliana, Monica Terenziani, Francesca Filippi, Alice Bergamini, Fabio Martinelli, Giorgia Mangili, Fedro Peccatori, Paolo Vercellini

Published in: Journal of Assisted Reproduction and Genetics | Issue 2/2019

Login to get access

Abstract

Chemotherapy during childhood damages ovarian reserve and can affect future fertility. However, recent large epidemiological studies showed that the detrimental impact on fertility is less severe if women seek for pregnancy at a younger age. To explain this observation, we hypothesize that the detrimental effects of previous chemotherapy on the ovarian reserve may be attenuated in young adults for two main reasons. Firstly, recent evidence showed that the amount of ovarian reserve is not a critical factor for effective natural conceptions. Provided that the residual ovarian reserve allows regular ovulatory cycles, the chances of pregnancy are similar in women with intact or reduced ovarian reserve. Secondly, ovarian reserve depletion appears to be a phenomenon that is inversely related to the residual ovarian reserve rather than to age. From a mathematical perspective, this kind of regulation intrinsically attenuates the effects of an early loss of a significant amount of primordial follicles. In conclusion, the detrimental effects of chemotherapy on natural fertility may be less severe if women with a history of chemotherapy during childhood seek for pregnancy early. This information should be part of the counseling.
Literature
1.
go back to reference Madanat LM, Malila N, Dyba T, Hakulinen T, Sankila R, Boice JD Jr, et al. Probability of parenthood after early onset cancer: a population-based study. Int J Cancer. 2008;123(12):2891–8.CrossRefPubMedPubMedCentral Madanat LM, Malila N, Dyba T, Hakulinen T, Sankila R, Boice JD Jr, et al. Probability of parenthood after early onset cancer: a population-based study. Int J Cancer. 2008;123(12):2891–8.CrossRefPubMedPubMedCentral
2.
go back to reference Reulen RC, Zeegers MP, Wallace WH, Frobisher C, Taylor AJ, Lancashire ER, et al. Pregnancy outcomes among adult survivors of childhood cancer in the British Childhood Cancer Survivor Study. Cancer Epidemiol Biomark Prev. 2009;18(8):2239–47.CrossRef Reulen RC, Zeegers MP, Wallace WH, Frobisher C, Taylor AJ, Lancashire ER, et al. Pregnancy outcomes among adult survivors of childhood cancer in the British Childhood Cancer Survivor Study. Cancer Epidemiol Biomark Prev. 2009;18(8):2239–47.CrossRef
3.
go back to reference Stensheim H, Cvancarova M, Møller B, Fosså SD. Pregnancy after adolescent and adult cancer: a population-based matched cohort study. Int J Cancer. 2011;129(5):1225–36.CrossRefPubMed Stensheim H, Cvancarova M, Møller B, Fosså SD. Pregnancy after adolescent and adult cancer: a population-based matched cohort study. Int J Cancer. 2011;129(5):1225–36.CrossRefPubMed
4.
go back to reference Pivetta E, Maule MM, Pisani P, Zugna D, Haupt R, Jankovic M, et al. Marriage and parenthood among childhood cancer survivors: a report from the Italian AIEOP Off-Therapy Registry. Haematologica. 2011;96(5):744–51.CrossRefPubMedPubMedCentral Pivetta E, Maule MM, Pisani P, Zugna D, Haupt R, Jankovic M, et al. Marriage and parenthood among childhood cancer survivors: a report from the Italian AIEOP Off-Therapy Registry. Haematologica. 2011;96(5):744–51.CrossRefPubMedPubMedCentral
5.
go back to reference Brämswig JH, Riepenhausen M, Schellong G. Parenthood in adult female survivors treated for Hodgkin’s lymphoma during childhood and adolescence: a prospective, longitudinal study. Lancet Oncol. 2015;16:667–75.CrossRefPubMed Brämswig JH, Riepenhausen M, Schellong G. Parenthood in adult female survivors treated for Hodgkin’s lymphoma during childhood and adolescence: a prospective, longitudinal study. Lancet Oncol. 2015;16:667–75.CrossRefPubMed
6.
go back to reference Chow EJ, Stratton KL, Leisenring WM, Oeffinger KC, Sklar CA, Donaldson SS, et al. Pregnancy after chemotherapy in male and female survivors of childhood cancer treated between 1970 and 1999: a report from the Childhood Cancer Survivor Study cohort. Lancet Oncol. 2016;17:567–76.CrossRefPubMedPubMedCentral Chow EJ, Stratton KL, Leisenring WM, Oeffinger KC, Sklar CA, Donaldson SS, et al. Pregnancy after chemotherapy in male and female survivors of childhood cancer treated between 1970 and 1999: a report from the Childhood Cancer Survivor Study cohort. Lancet Oncol. 2016;17:567–76.CrossRefPubMedPubMedCentral
7.
go back to reference Armuand G, Skoog-Svanberg A, Bladh M, Sydsjö G. Reproductive patterns among childhood and adolescent cancer survivors in Sweden: a population-based matched-cohort study. J Clin Oncol. 2017;35(14):1577–83.CrossRefPubMedPubMedCentral Armuand G, Skoog-Svanberg A, Bladh M, Sydsjö G. Reproductive patterns among childhood and adolescent cancer survivors in Sweden: a population-based matched-cohort study. J Clin Oncol. 2017;35(14):1577–83.CrossRefPubMedPubMedCentral
8.
go back to reference Anderson RA, Brewster DH, Wood R, Nowell S, Fischbacher C, Kelsey TW, et al. The impact of cancer on subsequent chance of pregnancy: a population-based analysis. Hum Reprod. 2018;33(7):1281–90.CrossRefPubMedPubMedCentral Anderson RA, Brewster DH, Wood R, Nowell S, Fischbacher C, Kelsey TW, et al. The impact of cancer on subsequent chance of pregnancy: a population-based analysis. Hum Reprod. 2018;33(7):1281–90.CrossRefPubMedPubMedCentral
9.
go back to reference van Dorp W, Haupt R, Anderson RA, Mulder RL, van den Heuvel-Eibrink MM, van Dulmen-den Broeder E, et al. Reproductive function and outcomes in female survivors of childhood, adolescent, and young adult cancer: a review. J Clin Oncol. 2018;36(21):2169–80.CrossRefPubMed van Dorp W, Haupt R, Anderson RA, Mulder RL, van den Heuvel-Eibrink MM, van Dulmen-den Broeder E, et al. Reproductive function and outcomes in female survivors of childhood, adolescent, and young adult cancer: a review. J Clin Oncol. 2018;36(21):2169–80.CrossRefPubMed
10.
go back to reference Morgan S, Anderson RA, Gourley C, Wallace WH, Spears N. How do chemotherapeutic agents damage the ovary? Hum Reprod Update. 2012;18:525–35.CrossRefPubMed Morgan S, Anderson RA, Gourley C, Wallace WH, Spears N. How do chemotherapeutic agents damage the ovary? Hum Reprod Update. 2012;18:525–35.CrossRefPubMed
11.
go back to reference Wallace WH, Kelsey TW, Anderson RA. Fertility preservation in pre-pubertal girls with cancer: the role of ovarian tissue cryopreservation. Fertil Steril. 2016;105:6–12.CrossRefPubMed Wallace WH, Kelsey TW, Anderson RA. Fertility preservation in pre-pubertal girls with cancer: the role of ovarian tissue cryopreservation. Fertil Steril. 2016;105:6–12.CrossRefPubMed
12.
go back to reference Oktem O, Kim SS, Selek U, Schatmann G, Urman B. Ovarian and Uterine functions in female survivors of childhood cancers. Oncologist. 2018;23:214–24.CrossRefPubMed Oktem O, Kim SS, Selek U, Schatmann G, Urman B. Ovarian and Uterine functions in female survivors of childhood cancers. Oncologist. 2018;23:214–24.CrossRefPubMed
13.
go back to reference Kalich-Philosoph L, Roness H, Carmely A, Fishel-Bartal M, Ligumsky H, Paglin S, et al. Cyclophosphamide triggers follicle activation and “burnout”; AS101 prevents follicle loss and preserves fertility. Sci Transl Med. 2013;5:185ra62.CrossRefPubMed Kalich-Philosoph L, Roness H, Carmely A, Fishel-Bartal M, Ligumsky H, Paglin S, et al. Cyclophosphamide triggers follicle activation and “burnout”; AS101 prevents follicle loss and preserves fertility. Sci Transl Med. 2013;5:185ra62.CrossRefPubMed
14.
go back to reference Meirow D, Dor J, Kaufman B, Shrim A, Rabinovici J, Schiff E, et al. Cortical fibrosis and blood-vessels damage in human ovaries exposed to chemotherapy. Potential mechanisms of ovarian injury. Hum Reprod. 2007;22(6):1626–33.CrossRefPubMed Meirow D, Dor J, Kaufman B, Shrim A, Rabinovici J, Schiff E, et al. Cortical fibrosis and blood-vessels damage in human ovaries exposed to chemotherapy. Potential mechanisms of ovarian injury. Hum Reprod. 2007;22(6):1626–33.CrossRefPubMed
16.
17.
go back to reference Mertes H. Let’s not forget that many prepubertal girls do have other options besides ovarian tissue cryopreservation. Hum Reprod. 2015;30:2011–3.CrossRefPubMed Mertes H. Let’s not forget that many prepubertal girls do have other options besides ovarian tissue cryopreservation. Hum Reprod. 2015;30:2011–3.CrossRefPubMed
18.
go back to reference Filippi F, Meazza C, Paffoni A, Raspagliesi F, Terenziani M, Somigliana E. Egg freezing in childhood and young adult cancer survivors. Pediatrics. 2016;138:e20160291.CrossRefPubMed Filippi F, Meazza C, Paffoni A, Raspagliesi F, Terenziani M, Somigliana E. Egg freezing in childhood and young adult cancer survivors. Pediatrics. 2016;138:e20160291.CrossRefPubMed
19.
go back to reference te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update. 2002;8:141–54.CrossRef te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update. 2002;8:141–54.CrossRef
20.
go back to reference Eijkemans MJ, van Poppel F, Habbema DF, Smith KR, Leridon H, te Velde ER. Too old to have children? Lessons from natural fertility populations. Hum Reprod. 2014;29:1304–12.CrossRefPubMedPubMedCentral Eijkemans MJ, van Poppel F, Habbema DF, Smith KR, Leridon H, te Velde ER. Too old to have children? Lessons from natural fertility populations. Hum Reprod. 2014;29:1304–12.CrossRefPubMedPubMedCentral
21.
go back to reference Navot D, Rosenwaks Z, Margalioth EJ. Prognostic assessment of female fecundity. Lancet. 1987;2:645–7.CrossRefPubMed Navot D, Rosenwaks Z, Margalioth EJ. Prognostic assessment of female fecundity. Lancet. 1987;2:645–7.CrossRefPubMed
22.
go back to reference Hagen CP, Vestergaard S, Juul A, Skakkebæk NE, Andersson AM, Main KM, et al. Low concentration of circulating antimullerian hormone is not predictive of reduced fecundability in young healthy women: a prospective cohort study. Fertil Steril. 2012;98:1602–8.CrossRefPubMed Hagen CP, Vestergaard S, Juul A, Skakkebæk NE, Andersson AM, Main KM, et al. Low concentration of circulating antimullerian hormone is not predictive of reduced fecundability in young healthy women: a prospective cohort study. Fertil Steril. 2012;98:1602–8.CrossRefPubMed
23.
go back to reference Streuli I, de Mouzon J, Paccolat C, Chapron C, Petignat P, Irion OP, et al. AMH concentration is not related to effective time to pregnancy in women who conceive naturally. Reprod BioMed Online. 2014;28:216–24.CrossRefPubMed Streuli I, de Mouzon J, Paccolat C, Chapron C, Petignat P, Irion OP, et al. AMH concentration is not related to effective time to pregnancy in women who conceive naturally. Reprod BioMed Online. 2014;28:216–24.CrossRefPubMed
24.
go back to reference Somigliana E, Lattuada D, Colciaghi B, Filippi F, La Vecchia I, Tirelli A, et al. Serum anti-Mullerian hormone in subfertile women. Acta Obstet Gynecol Scand. 2015;94:1307–12.CrossRefPubMed Somigliana E, Lattuada D, Colciaghi B, Filippi F, La Vecchia I, Tirelli A, et al. Serum anti-Mullerian hormone in subfertile women. Acta Obstet Gynecol Scand. 2015;94:1307–12.CrossRefPubMed
25.
go back to reference Steiner AZ, Pritchard D, Stanczyk FZ, Kesner JS, Meadows JW, Herring AH, et al. Association between biomarkers of ovarian reserve and infertility among older women of reproductive age. JAMA. 2017;318:1367–76.CrossRefPubMedPubMedCentral Steiner AZ, Pritchard D, Stanczyk FZ, Kesner JS, Meadows JW, Herring AH, et al. Association between biomarkers of ovarian reserve and infertility among older women of reproductive age. JAMA. 2017;318:1367–76.CrossRefPubMedPubMedCentral
26.
go back to reference Greenwood EA, Cedars MI, Santoro N, Eisenberg E, Kao CN, Haisenleder DJ, et al. Antimüllerian hormone levels and antral follicle counts are not reduced compared with community controls in patients with rigorously defined unexplained infertility. Fertil Steril. 2017;108(6):1070–7.CrossRefPubMed Greenwood EA, Cedars MI, Santoro N, Eisenberg E, Kao CN, Haisenleder DJ, et al. Antimüllerian hormone levels and antral follicle counts are not reduced compared with community controls in patients with rigorously defined unexplained infertility. Fertil Steril. 2017;108(6):1070–7.CrossRefPubMed
27.
go back to reference Daan NM, Hoek A, Corpeleijn E, Eijkemans MJ, Broekmans FJ, Fauser BC, et al. Reproductive characteristics of women diagnosed with premature ovarian insufficiency. Reprod BioMed Online. 2016;32:225–32.CrossRefPubMed Daan NM, Hoek A, Corpeleijn E, Eijkemans MJ, Broekmans FJ, Fauser BC, et al. Reproductive characteristics of women diagnosed with premature ovarian insufficiency. Reprod BioMed Online. 2016;32:225–32.CrossRefPubMed
28.
go back to reference Letourneau JM, Ebbel EE, Katz PP, Oktay KH, McCulloch CE, Ai WZ, et al. Acute ovarian failure underestimates age-specific reproductive impairment for young women undergoing chemotherapy for cancer. Cancer. 2012;118:1933–9.CrossRefPubMed Letourneau JM, Ebbel EE, Katz PP, Oktay KH, McCulloch CE, Ai WZ, et al. Acute ovarian failure underestimates age-specific reproductive impairment for young women undergoing chemotherapy for cancer. Cancer. 2012;118:1933–9.CrossRefPubMed
29.
go back to reference Oktem O, Oktay K. A novel ovarian xenografting model to characterize the impact of chemotherapy agents on human primordial follicle reserve. Cancer Res. 2007;67:10159–62.CrossRefPubMed Oktem O, Oktay K. A novel ovarian xenografting model to characterize the impact of chemotherapy agents on human primordial follicle reserve. Cancer Res. 2007;67:10159–62.CrossRefPubMed
30.
go back to reference Soleimani R, Heytens E, Darzynkiewicz Z, Oktay K. Mechanisms of chemotherapy-induced human ovarian aging: double strand DNA breaks and microvascular compromise. Aging. 2011;3:782–93.CrossRefPubMedPubMedCentral Soleimani R, Heytens E, Darzynkiewicz Z, Oktay K. Mechanisms of chemotherapy-induced human ovarian aging: double strand DNA breaks and microvascular compromise. Aging. 2011;3:782–93.CrossRefPubMedPubMedCentral
31.
go back to reference Oktem O, Oktay K. Quantitative assessment of the impact of chemotherapy on ovarian follicle reserve and stromal function. Cancer. 2007;110:2222–9.CrossRefPubMed Oktem O, Oktay K. Quantitative assessment of the impact of chemotherapy on ovarian follicle reserve and stromal function. Cancer. 2007;110:2222–9.CrossRefPubMed
32.
go back to reference McLaughlin M, Kelsey TW, Wallace WH, Anderson RA, Telfer EE. Non-growing follicle density is increased following adriamycin, bleomycin, vinblastine and dacarbazine (ABVD) chemotherapy in the adult human ovary. Hum Reprod. 2017;32:165–74.PubMed McLaughlin M, Kelsey TW, Wallace WH, Anderson RA, Telfer EE. Non-growing follicle density is increased following adriamycin, bleomycin, vinblastine and dacarbazine (ABVD) chemotherapy in the adult human ovary. Hum Reprod. 2017;32:165–74.PubMed
33.
go back to reference Lie Fong S, Laven JS, Hakvoort-Cammel FG, Schipper I, Visser JA, Themmen AP, et al. Assessment of ovarian reserve in adult childhood cancer survivors using anti-Müllerian hormone. Hum Reprod. 2009;24:982–90.CrossRefPubMed Lie Fong S, Laven JS, Hakvoort-Cammel FG, Schipper I, Visser JA, Themmen AP, et al. Assessment of ovarian reserve in adult childhood cancer survivors using anti-Müllerian hormone. Hum Reprod. 2009;24:982–90.CrossRefPubMed
34.
go back to reference Gracia CR, Sammel MD, Freeman E, Prewitt M, Carlson C, Ray A, et al. Impact of cancer therapies on ovarian reserve. Fertil Steril. 2012;97:134–40.CrossRefPubMed Gracia CR, Sammel MD, Freeman E, Prewitt M, Carlson C, Ray A, et al. Impact of cancer therapies on ovarian reserve. Fertil Steril. 2012;97:134–40.CrossRefPubMed
35.
go back to reference Dillon KE, Sammel MD, Ginsberg JP, Lechtenberg L, Prewitt M, Gracia CR. Pregnancy after cancer: results from a prospective cohort study of cancer survivors. Pediatr Blood Cancer. 2013;60:2001–6.CrossRefPubMedPubMedCentral Dillon KE, Sammel MD, Ginsberg JP, Lechtenberg L, Prewitt M, Gracia CR. Pregnancy after cancer: results from a prospective cohort study of cancer survivors. Pediatr Blood Cancer. 2013;60:2001–6.CrossRefPubMedPubMedCentral
36.
go back to reference El-Shalakany AH, Ali MS, Abdelmaksoud AA, Abd El-Ghany S, Hasan EA. Ovarian function in female survivors of childhood malignancies. Pediatr Hematol Oncol. 2013;30:328–35.CrossRefPubMed El-Shalakany AH, Ali MS, Abdelmaksoud AA, Abd El-Ghany S, Hasan EA. Ovarian function in female survivors of childhood malignancies. Pediatr Hematol Oncol. 2013;30:328–35.CrossRefPubMed
37.
go back to reference Krawczuk-Rybak M, Leszczynska E, Poznanska M, Zelazowska-Rutkowska B, Wysocka J. Anti-müllerian hormone as a sensitive marker of ovarian function in young cancer survivors. Int J Endocrinol. 2013;2013:125080.CrossRefPubMedPubMedCentral Krawczuk-Rybak M, Leszczynska E, Poznanska M, Zelazowska-Rutkowska B, Wysocka J. Anti-müllerian hormone as a sensitive marker of ovarian function in young cancer survivors. Int J Endocrinol. 2013;2013:125080.CrossRefPubMedPubMedCentral
38.
go back to reference Johnson LN, Sammel MD, Dillon KE, Lechtenberg L, Schanne A, Gracia CR. Antimüllerian hormone and antral follicle count are lower in female cancer survivors and healthy women taking hormonal contraception. Fertil Steril. 2014;102:774–81.CrossRefPubMedPubMedCentral Johnson LN, Sammel MD, Dillon KE, Lechtenberg L, Schanne A, Gracia CR. Antimüllerian hormone and antral follicle count are lower in female cancer survivors and healthy women taking hormonal contraception. Fertil Steril. 2014;102:774–81.CrossRefPubMedPubMedCentral
39.
go back to reference Akar B, Doğer E, Çakıroğlu Y, Çorapçıoğlu F, Sarper N, Çalışkan E. The effect of childhood cancer therapy on ovarian reserve and pubertal development. Reprod BioMed Online. 2015;30:175–80.CrossRefPubMed Akar B, Doğer E, Çakıroğlu Y, Çorapçıoğlu F, Sarper N, Çalışkan E. The effect of childhood cancer therapy on ovarian reserve and pubertal development. Reprod BioMed Online. 2015;30:175–80.CrossRefPubMed
40.
go back to reference Thomas-Teinturier C, Allodji RS, Svetlova E, Frey MA, Oberlin O, Millischer AE, et al. Ovarian reserve after treatment with alkylating agents during childhood. Hum Reprod. 2015;30:1437–46.CrossRefPubMed Thomas-Teinturier C, Allodji RS, Svetlova E, Frey MA, Oberlin O, Millischer AE, et al. Ovarian reserve after treatment with alkylating agents during childhood. Hum Reprod. 2015;30:1437–46.CrossRefPubMed
41.
go back to reference Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum Reprod. 1992;7:1342–6.CrossRefPubMed Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum Reprod. 1992;7:1342–6.CrossRefPubMed
42.
go back to reference 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;72:845–51.CrossRefPubMed 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;72:845–51.CrossRefPubMed
43.
go back to reference Hanson B. Questioning the construction of maternal age as a fertility problem. Health Care Women Int. 2003;24:166–76.CrossRefPubMed Hanson B. Questioning the construction of maternal age as a fertility problem. Health Care Women Int. 2003;24:166–76.CrossRefPubMed
44.
go back to reference Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR, Klein NA. A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod. 2008;23:699–708.CrossRefPubMed Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR, Klein NA. A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod. 2008;23:699–708.CrossRefPubMed
45.
go back to reference Rosen MP, Sternfeld B, Schuh-Huerta SM, Reijo Pera RA, McCulloch CE, Cedars MI. Antral follicle count: absence of significant midlife decline. Fertil Steril. 2010;94:2182–5.CrossRefPubMedPubMedCentral Rosen MP, Sternfeld B, Schuh-Huerta SM, Reijo Pera RA, McCulloch CE, Cedars MI. Antral follicle count: absence of significant midlife decline. Fertil Steril. 2010;94:2182–5.CrossRefPubMedPubMedCentral
47.
go back to reference Kelsey TW, Anderson RA, Wright P, et al. Data-driven assessment of the human ovarian reserve. Mol Hum Reprod. 2012;18:79–87.CrossRefPubMed Kelsey TW, Anderson RA, Wright P, et al. Data-driven assessment of the human ovarian reserve. Mol Hum Reprod. 2012;18:79–87.CrossRefPubMed
48.
go back to reference Wallace WH, Smith AG, Kelsey TW, Nelson SM, Wallace WH. Fertility preservation for girls and young women with cancer: population-based validation of criteria for ovarian tissue cryopreservation. Lancet Oncol. 2014;15:1129–36.CrossRefPubMedPubMedCentral Wallace WH, Smith AG, Kelsey TW, Nelson SM, Wallace WH. Fertility preservation for girls and young women with cancer: population-based validation of criteria for ovarian tissue cryopreservation. Lancet Oncol. 2014;15:1129–36.CrossRefPubMedPubMedCentral
49.
go back to reference Mills M, Rindfuss RR, McDonald P, te Velde E, ESHRE Reproduction and Society Task Force. Why do people postpone parenthood? Reasons and social policy incentives. Hum Reprod Update. 2011;17:848–60.CrossRefPubMedPubMedCentral Mills M, Rindfuss RR, McDonald P, te Velde E, ESHRE Reproduction and Society Task Force. Why do people postpone parenthood? Reasons and social policy incentives. Hum Reprod Update. 2011;17:848–60.CrossRefPubMedPubMedCentral
50.
go back to reference van Dijk M, van den Berg MH, Overbeek A, Lambalk CB, van den Heuvel-Eibrink MM, Tissing WJ, et al. Reproductive intentions and use of reproductive health care among female survivors of childhood cancer. Hum Reprod. 2018;33(6):1167–74.CrossRefPubMed van Dijk M, van den Berg MH, Overbeek A, Lambalk CB, van den Heuvel-Eibrink MM, Tissing WJ, et al. Reproductive intentions and use of reproductive health care among female survivors of childhood cancer. Hum Reprod. 2018;33(6):1167–74.CrossRefPubMed
51.
go back to reference Sunkara SK, Rittenberg V, Raine-Fenning N, Bhattacharya S, Zamora J, Coomarasamy A. Association between the number of eggs and live birth in IVF treatment: an analysis of 400 135 treatment cycles. Hum Reprod. 2011;26:1768–74.CrossRefPubMed Sunkara SK, Rittenberg V, Raine-Fenning N, Bhattacharya S, Zamora J, Coomarasamy A. Association between the number of eggs and live birth in IVF treatment: an analysis of 400 135 treatment cycles. Hum Reprod. 2011;26:1768–74.CrossRefPubMed
52.
go back to reference Kelsey TW, Wright P, Nelson SM, Anderson RA, Wallace WH. A validated model of serum anti-müllerian hormone from conception to menopause. PLoS One. 2011;6(7):e22024.CrossRefPubMedPubMedCentral Kelsey TW, Wright P, Nelson SM, Anderson RA, Wallace WH. A validated model of serum anti-müllerian hormone from conception to menopause. PLoS One. 2011;6(7):e22024.CrossRefPubMedPubMedCentral
53.
go back to reference Zamah AM, Stephenson MD. Antimüllerian hormone and miscarriage: fifty shadesof gray. Fertil Steril. 2018;109:1008–9.CrossRefPubMed Zamah AM, Stephenson MD. Antimüllerian hormone and miscarriage: fifty shadesof gray. Fertil Steril. 2018;109:1008–9.CrossRefPubMed
54.
go back to reference Lyttle Schumacher BM, Jukic AMZ, Steiner AZ. Antimüllerian hormone as a risk factor for miscarriage in naturally conceived pregnancies. Fertil Steril. 2018;109(6):1065–71.CrossRefPubMedPubMedCentral Lyttle Schumacher BM, Jukic AMZ, Steiner AZ. Antimüllerian hormone as a risk factor for miscarriage in naturally conceived pregnancies. Fertil Steril. 2018;109(6):1065–71.CrossRefPubMedPubMedCentral
Metadata
Title
Chemotherapy-related damage to ovarian reserve in childhood cancer survivors: interpreting the evidence
Authors
Edgardo Somigliana
Monica Terenziani
Francesca Filippi
Alice Bergamini
Fabio Martinelli
Giorgia Mangili
Fedro Peccatori
Paolo Vercellini
Publication date
01-02-2019
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 2/2019
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-018-1345-8

Other articles of this Issue 2/2019

Journal of Assisted Reproduction and Genetics 2/2019 Go to the issue