Review
. 2020 Oct; 21(20):7792.
doi: 10.3390/ijms21207792.

Advances in the Treatment and Prevention of Chemotherapy-Induced Ovarian Toxicity

Hyun-Woong Cho 1 Sanghoon Lee 1 Kyung-Jin Min 1 Jin Hwa Hong 1 Jae Yun Song 1 Jae Kwan Lee 1 Nak Woo Lee 1 Tak Kim 1 
Affiliations
  • PMID: 33096794
  •     181 References

Abstract

Due to improvements in chemotherapeutic agents, cancer treatment efficacy and cancer patient survival rates have greatly improved, but unfortunately gonadal damage remains a major complication. Gonadotoxic chemotherapy, including alkylating agents during reproductive age, can lead to iatrogenic premature ovarian insufficiency (POI), and loss of fertility. In recent years, the demand for fertility preservation has increased dramatically among female cancer patients. Currently, embryo and oocyte cryopreservation are the only established options for fertility preservation in women. However, there is growing evidence for other experimental techniques including ovarian tissue cryopreservation, oocyte in vitro maturation, artificial ovaries, stem cell technologies, and ovarian suppression. To prevent fertility loss in women with cancer, individualized fertility preservation options including established and experimental techniques that take into consideration the patient's age, marital status, chemotherapy regimen, and the possibility of treatment delay should be provided. In addition, effective multidisciplinary oncofertility strategies that involve a highly skilled and experienced oncofertility team consisting of medical oncologists, gynecologists, reproductive biologists, surgical oncologists, patient care coordinators, and research scientists are necessary to provide cancer patients with high-quality care.

Keywords: artificial ovaries; embryo cryopreservation; fertility preservation; gonadotoxicity; oncofertility; oocyte cryopreservation; oocyte in vitro maturation; ovarian suppression; ovarian tissue cryopreservation; stem cell technologies.

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Stephanie K Petrillo, Patrice Desmeules, To-Quyen Truong, Patrick J Devine.
Toxicol Appl Pharmacol, 2011 Mar 29; 253(2). PMID: 21439308
Long-term follow up of ovarian function in women treated with MOPP chemotherapy for Hodgkin's disease.
R L Schilsky, R J Sherins, +3 authors, V T DeVita.
Am J Med, 1981 Oct 01; 71(4). PMID: 7282743
Ninety-five orthotopic transplantations in 74 women of ovarian tissue after cytotoxic treatment in a fertility preservation network: tissue activity, pregnancy and delivery rates.
H Van der Ven, J Liebenthron, +17 authors, FertiPROTEKT network.
Hum Reprod, 2016 Jul 06; 31(9). PMID: 27378768
Highly Cited.
Efficiency of aseptic open vitrification and hermetical cryostorage of human oocytes.
L Parmegiani, G E Cognigni, +7 authors, M Filicori.
Reprod Biomed Online, 2011 Aug 17; 23(4). PMID: 21843968
Transplantation of an alginate-matrigel matrix containing isolated ovarian cells: first step in developing a biodegradable scaffold to transplant isolated preantral follicles and ovarian cells.
Julie Vanacker, Valérie Luyckx, +5 authors, Christiani A Amorim.
Biomaterials, 2012 Jun 05; 33(26). PMID: 22658800
Comparison between Slow Freezing and Vitrification for Human Ovarian Tissue Cryopreservation and Xenotransplantation.
Sanghoon Lee, Ki-Jin Ryu, +3 authors, Tak Kim.
Int J Mol Sci, 2019 Jul 11; 20(13). PMID: 31288388    Free PMC article.
Effect of the gonadotropin-releasing hormone analogue triptorelin on the occurrence of chemotherapy-induced early menopause in premenopausal women with breast cancer: a randomized trial.
Lucia Del Mastro, Luca Boni, +14 authors, Marco Venturini.
JAMA, 2011 Jul 21; 306(3). PMID: 21771987
The best source of isolated stromal cells for the artificial ovary: medulla or cortex, cryopreserved or fresh?
M Soares, K Sahrari, +4 authors, M-M Dolmans.
Hum Reprod, 2015 May 23; 30(7). PMID: 25994668
Role of SDF-1/CXCR4 and cytokines in the development of ovary injury in chemotherapy drug induced premature ovarian failure mice.
Qianqian Luo, Na Yin, +4 authors, Hongqin Zhang.
Life Sci, 2017 May 10; 179. PMID: 28478265
Human ovarian tissue vitrification versus conventional freezing: morphological, endocrinological, and molecular biological evaluation.
V Isachenko, I Lapidus, +5 authors, J M Weiss.
Reproduction, 2009 May 15; 138(2). PMID: 19439559
Fertility preservation in women with cancer.
Sanghoon Lee, Jae Yun Song, +2 authors, Tak Kim.
Clin Exp Reprod Med, 2012 Jul 21; 39(2). PMID: 22816069    Free PMC article.
In vitro maturation of human immature oocytes for fertility preservation.
Ri-Cheng Chian, Peter S Uzelac, Geeta Nargund.
Fertil Steril, 2013 Feb 26; 99(5). PMID: 23433515
Review.
Cancer treatment and gonadal function: experimental and established strategies for fertility preservation in children and young adults.
Richard A Anderson, Rod T Mitchell, +3 authors, W Hamish B Wallace.
Lancet Diabetes Endocrinol, 2015 Apr 16; 3(7). PMID: 25873571
Highly Cited. Review.
The Oncofertility Consortium--addressing fertility in young people with cancer.
Teresa K Woodruff.
Nat Rev Clin Oncol, 2010 May 26; 7(8). PMID: 20498666    Free PMC article.
Review.
Fertility issues in patients with hematologic malignancies.
Alison W Loren.
Hematology Am Soc Hematol Educ Program, 2015 Dec 08; 2015. PMID: 26637713
Review.
Psychological Counseling of Female Fertility Preservation Patients.
Angela K Lawson, Susan C Klock, +3 authors, Ralph R Kazer.
J Psychosoc Oncol, 2015 May 23; 33(4). PMID: 25996581    Free PMC article.
Review.
Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation.
Jacques Donnez, Marie-Madeleine Dolmans, +6 authors, Claus Yding Andersen.
Fertil Steril, 2013 May 03; 99(6). PMID: 23635349
Highly Cited. Review.
In Vitro Maturation in Women with vs. without Polycystic Ovarian Syndrome: A Systematic Review and Meta-Analysis.
Charalampos Siristatidis, Theodoros N Sergentanis, +4 authors, Theodora Psaltopoulou.
PLoS One, 2015 Aug 05; 10(8). PMID: 26241855    Free PMC article.
Systematic Review.
The radiosensitivity of the human oocyte.
W H B Wallace, A B Thomson, T W Kelsey.
Hum Reprod, 2003 Jan 15; 18(1). PMID: 12525451
Duration of storage of cryopreserved human embryos.
J Cohen, K L Inge, +3 authors, T G Turner.
J In Vitro Fert Embryo Transf, 1988 Oct 01; 5(5). PMID: 3230354
Embryo development of fresh 'versus' vitrified metaphase II oocytes after ICSI: a prospective randomized sibling-oocyte study.
Laura Rienzi, Stefania Romano, +6 authors, Filippo Ubaldi.
Hum Reprod, 2009 Oct 29; 25(1). PMID: 19861328    Free PMC article.
Comparison of survival and embryonic development in human oocytes cryopreserved by slow-freezing and vitrification.
Yun-Xia Cao, Qiong Xing, +4 authors, Ping Zhou.
Fertil Steril, 2008 Oct 22; 92(4). PMID: 18930218
Preserving fertility in female patients with hematological malignancies: a multidisciplinary oncofertility approach.
M Salama, A Anazodo, T K Woodruff.
Ann Oncol, 2019 Aug 17; 30(11). PMID: 31418765
Review.
Ovarian Follicle Depletion Induced by Chemotherapy and the Investigational Stages of Potential Fertility-Protective Treatments-A Review.
Xia Hao, Amandine Anastácio, Kui Liu, Kenny A Rodriguez-Wallberg.
Int J Mol Sci, 2019 Sep 25; 20(19). PMID: 31548505    Free PMC article.
Review.
Luteal phase oocyte retrieval and in vitro maturation is an optional procedure for urgent fertility preservation.
Ettie Maman, Dror Meirow, +3 authors, Ariel Hourvitz.
Fertil Steril, 2010 Aug 07; 95(1). PMID: 20688325
Updates in preserving reproductive potential of prepubertal girls with cancer: Systematic review.
Mahmoud Salama, Vladimir Isachenko, +2 authors, Peter Mallmann.
Crit Rev Oncol Hematol, 2016 May 18; 103. PMID: 27184425
Systematic Review.
The effects of radiotherapy and chemotherapy on female reproduction.
D Meirow, D Nugent.
Hum Reprod Update, 2001 Dec 01; 7(6). PMID: 11727861
Highly Cited. Review.
Comments on the letter "Fertility preservation and GnRHa for chemotherapy: debate".
Michael von Wolff, Juliane Raddatz, +3 authors, Markus Nitzschke.
Arch Gynecol Obstet, 2010 Apr 30; 282(6). PMID: 20428880
Ovarian regeneration: The potential for stem cell contribution in the postnatal ovary to sustained endocrine function.
Alisha M Truman, Jonathan L Tilly, Dori C Woods.
Mol Cell Endocrinol, 2016 Oct 17; 445. PMID: 27743990    Free PMC article.
Review.
Prospective study of fertility concerns and preservation strategies in young women with breast cancer.
Kathryn J Ruddy, Shari I Gelber, +6 authors, Ann H Partridge.
J Clin Oncol, 2014 Feb 26; 32(11). PMID: 24567428    Free PMC article.
Highly Cited.
How to preserve fertility in young women exposed to chemotherapy? The role of GnRH agonist cotreatment in addition to cryopreservation of embrya, oocytes, or ovaries.
Zeev Blumenfeld.
Oncologist, 2007 Oct 05; 12(9). PMID: 17914074
Review.
Effective method for emergency fertility preservation: random-start controlled ovarian stimulation.
Hakan Cakmak, Audra Katz, Marcelle I Cedars, Mitchell P Rosen.
Fertil Steril, 2013 Aug 31; 100(6). PMID: 23987516
Ovarian tissue cryopreservation in young cancer patients for fertility preservation.
Nao Suzuki.
Reprod Med Biol, 2014 Jul 18; 14(1). PMID: 29259397    Free PMC article.
Review.
Preservation of fertility in females with haematological malignancy.
Jacques Donnez, Marie-Madeleine Dolmans.
Br J Haematol, 2011 May 14; 154(2). PMID: 21564077
Review.
Random-start ovarian stimulation in patients with cancer.
Hakan Cakmak, Mitchell P Rosen.
Curr Opin Obstet Gynecol, 2015 Apr 29; 27(3). PMID: 25919235
Review.
IVM results are comparable and may have advantages over standard IVF.
A Ellenbogen, T Shavit, E Shalom-Paz.
Facts Views Vis Obgyn, 2014 Jul 11; 6(2). PMID: 25009730    Free PMC article.
Review.
Creating a Global Community of Practice for Oncofertility.
Lauren M Ataman, Jhenifer K Rodrigues, +47 authors, Teresa K Woodruff.
J Glob Oncol, 2016 Jun 11; 2(2). PMID: 27284576    Free PMC article.
Evidence of residual disease in cryopreserved ovarian cortex from female patients with leukemia.
Mikkel Rosendahl, Morten Tolstrup Andersen, +3 authors, Claus Yding Andersen.
Fertil Steril, 2010 Jan 27; 94(6). PMID: 20100619
Fresh versus Frozen Embryos for Infertility in the Polycystic Ovary Syndrome.
Zi-Jiang Chen, Yuhua Shi, +19 authors, Richard S Legro.
N Engl J Med, 2016 Aug 11; 375(6). PMID: 27509101
Highly Cited.
Cisplatin- and cyclophosphamide-induced primordial follicle depletion is caused by direct damage to oocytes.
Q N Nguyen, N Zerafa, +3 authors, K J Hutt.
Mol Hum Reprod, 2019 Apr 07; 25(8). PMID: 30953068
Trends of socioeconomic disparities in referral patterns for fertility preservation consultation.
Linnea R Goodman, Ursula Balthazar, Jayeon Kim, Jennifer E Mersereau.
Hum Reprod, 2012 May 04; 27(7). PMID: 22552688    Free PMC article.
Absence of conclusive evidence for the safety and efficacy of gonadotropin-releasing hormone analogue treatment in protecting against chemotherapy-induced gonadal injury.
Kutluk Oktay, Murat Sönmezer, +3 authors, Heejung Bang.
Oncologist, 2007 Oct 05; 12(9). PMID: 17914075
Review.
First pregnancy and live birth resulting from cryopreserved embryos obtained from in vitro matured oocytes after oophorectomy in an ovarian cancer patient.
E B Prasath, M L H Chan, +5 authors, Y N Chia.
Hum Reprod, 2013 Dec 12; 29(2). PMID: 24327539
Management of fertility in patients treated for Hodgkin's lymphoma.
Stephanie Harel, Christophe Fermé, Catherine Poirot.
Haematologica, 2011 Aug 11; 96(11). PMID: 21828120    Free PMC article.
Review.
Hydrogel network design using multifunctional macromers to coordinate tissue maturation in ovarian follicle culture.
Ariella Shikanov, Rachel M Smith, +2 authors, Lonnie D Shea.
Biomaterials, 2011 Jan 21; 32(10). PMID: 21247629    Free PMC article.
Utilization rates and results of long-term embryo cryopreservation before gonadotoxic treatment.
M M Dolmans, S Hollanders de Ouderaen, D Demylle, C Pirard.
J Assist Reprod Genet, 2015 Jul 16; 32(8). PMID: 26174124    Free PMC article.
Live birth from a frozen-thawed pronuclear stage embryo almost 20 years after its cryopreservation.
Donna Dowling-Lacey, Jacob F Mayer, +3 authors, Sergio Oehninger.
Fertil Steril, 2010 Oct 05; 95(3). PMID: 20887984
Fertility issues in cancer survivorship.
Jonathan D Kort, Michael L Eisenberg, Leah S Millheiser, Lynn M Westphal.
CA Cancer J Clin, 2014 Mar 08; 64(2). PMID: 24604743
Review.
Purification of germline stem cells from adult mammalian ovaries: a step closer towards control of the female biological clock?
Jonathan L Tilly, Evelyn E Telfer.
Mol Hum Reprod, 2009 Jun 11; 15(7). PMID: 19509111    Free PMC article.
In vitro maturation of human immature oocytes for fertility preservation and research material.
Hiromitsu Shirasawa, Yukihiro Terada.
Reprod Med Biol, 2017 Dec 21; 16(3). PMID: 29259476    Free PMC article.
Review.
Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
Freddie Bray, Jacques Ferlay, +3 authors, Ahmedin Jemal.
CA Cancer J Clin, 2018 Sep 13; 68(6). PMID: 30207593
Highly Cited.
American Society of Clinical Oncology recommendations on fertility preservation in cancer patients.
Stephanie J Lee, Leslie R Schover, +7 authors, American Society of Clinical Oncology.
J Clin Oncol, 2006 May 03; 24(18). PMID: 16651642
Highly Cited. Systematic Review.
Fertility status among women treated for aggressive non-Hodgkin's lymphoma.
Avishay Elis, Aharon Tevet, +8 authors, Michael Lishner.
Leuk Lymphoma, 2006 May 13; 47(4). PMID: 16690520
Oocyte cryopreservation: where are we now?
Catrin E Argyle, Joyce C Harper, Melanie C Davies.
Hum Reprod Update, 2016 Mar 24; 22(4). PMID: 27006004
Review.
Slow-freezing versus vitrification for human ovarian tissue cryopreservation.
Silke Klocke, Nana Bündgen, +2 authors, Georg Griesinger.
Arch Gynecol Obstet, 2014 Aug 15; 291(2). PMID: 25115279
Early menopause in long-term survivors of cancer during adolescence.
J Byrne, T R Fears, +7 authors, J W Meigs.
Am J Obstet Gynecol, 1992 Mar 01; 166(3). PMID: 1550144
Cryopreserved ovarian cortex from patients with leukemia in complete remission contains no apparent viable malignant cells.
Tine Greve, Erik Clasen-Linde, +5 authors, Claus Yding Andersen.
Blood, 2012 Jun 20; 120(22). PMID: 22709693
Final Analysis of the Prevention of Early Menopause Study (POEMS)/SWOG Intergroup S0230.
Halle C F Moore, Joseph M Unger, +22 authors, Kathy S Albain.
J Natl Cancer Inst, 2018 Oct 30; 111(2). PMID: 30371800    Free PMC article.
Prospective randomized comparison of human oocyte cryopreservation with slow-rate freezing or vitrification.
Gary D Smith, Paulo C Serafini, +5 authors, Eduardo L Motta.
Fertil Steril, 2010 Feb 23; 94(6). PMID: 20171613
UK lifts ban on frozen eggs.
J Wise.
BMJ, 2000 Feb 05; 320(7231). PMID: 10657318    Free PMC article.
Fertility preservation for age-related fertility decline.
Dominic Stoop, Ana Cobo, Sherman Silber.
Lancet, 2014 Oct 07; 384(9950). PMID: 25283572
Review.
Transplantations of frozen-thawed ovarian tissue demonstrate high reproductive performance and the need to revise restrictive criteria.
Dror Meirow, Hila Ra'anani, +7 authors, Jehoshua Dor.
Fertil Steril, 2016 May 18; 106(2). PMID: 27181924
Fertility preservation for age-related fertility decline.
Jacques Donnez, Marie-Madeleine Dolmans, +4 authors, Claus Yding Andersen.
Lancet, 2015 Feb 24; 385(9967). PMID: 25705839
GnRH analogs do not protect ovaries from chemotherapy-induced ultrastructural injury in Hodgkin's lymphoma patients.
Markus Nitzschke, Juliane Raddatz, +3 authors, Michael von Wolff.
Arch Gynecol Obstet, 2009 Dec 08; 282(1). PMID: 19967405
In Vitro Generation of Oocytes from Ovarian Stem Cells (OSCs): In Search of Major Evidence.
Erica Silvestris, Stella D'Oronzo, +3 authors, Gennaro Cormio.
Int J Mol Sci, 2019 Dec 15; 20(24). PMID: 31835581    Free PMC article.
Review.
Cancer, fertility and pregnancy: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up.
G Pentheroudakis, R Orecchia, +2 authors, ESMO Guidelines Working Group.
Ann Oncol, 2010 Jun 29; 21 Suppl 5. PMID: 20555095
Ovarian failure in long-term survivors of childhood malignancy.
R J Stillman, J S Schinfeld, +5 authors, F P Li.
Am J Obstet Gynecol, 1981 Jan 01; 139(1). PMID: 7457523
In vitro maturation of immature human oocytes for clinical application.
Ri-Cheng Chian, Yun-Xia Cao.
Methods Mol Biol, 2014 May 02; 1154. PMID: 24782014
LH prevents cisplatin-induced apoptosis in oocytes and preserves female fertility in mouse.
Valerio Rossi, Monica Lispi, +5 authors, Francesca G Klinger.
Cell Death Differ, 2016 Oct 01; 24(1). PMID: 27689876    Free PMC article.
Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update.
Alison W Loren, Pamela B Mangu, +7 authors, American Society of Clinical Oncology.
J Clin Oncol, 2013 May 30; 31(19). PMID: 23715580    Free PMC article.
Highly Cited. Systematic Review.
Fertility preservation in >1,000 patients: patient's characteristics, spectrum, efficacy and risks of applied preservation techniques.
Barbara Lawrenz, Julia Jauckus, +2 authors, Michael von Wolff.
Arch Gynecol Obstet, 2010 Dec 02; 283(3). PMID: 21120512