Impact of adjuvant chemotherapy or tamoxifen-alone on the ovarian reserve of young women with breast cancer.
Anti-mullerian hormone
Breast neoplasms
Drug therapy
Fertility preservation
Ovarian reserve
Journal
Breast cancer research and treatment
ISSN: 1573-7217
Titre abrégé: Breast Cancer Res Treat
Pays: Netherlands
ID NLM: 8111104
Informations de publication
Date de publication:
Jan 2021
Jan 2021
Historique:
received:
31
07
2020
accepted:
05
09
2020
pubmed:
16
9
2020
medline:
24
6
2021
entrez:
15
9
2020
Statut:
ppublish
Résumé
To determine the longitudinal impact of adjuvant chemotherapy and tamoxifen-only treatments on the reproductive potential of women with breast cancer by using a sensitive ovarian reserve marker anti-Mullerian hormone (AMH) as a surrogate. One-hundred-and-forty-two women with a primary diagnosis of breast cancer were prospectively followed with serum AMH assessments before the initiation, and 12, 18 and 24 months after the completion of adjuvant chemotherapy or the start of tamoxifen-only treatment. The chemotherapy regimens were classified into Anthracycline-Cyclophosphamide-based (AC-based) and Cyclophosphamide-Methotrexate + 5-Fluorouracil (CMF). Longitudinal data were analyzed by mixed effects model for treatment effects over time, adjusting for baseline age and BMI. Both chemotherapy regimens resulted in significant decline in ovarian reserve compared to the tamoxifen-only treatment (p < 0.0001 either regimen vs. tamoxifen for overall trend). AMH levels sharply declined at 12 months but did not show a significant recovery from 12 to 18 and 18 to 24 months after the completion of AC-based or CMF regimens. The degree of decline did not differ between the two chemotherapy groups (p = 0.53). In contrast, tamoxifen-only treatment did not significantly alter the age-adjusted serum AMH levels over the 24-month follow up. Likewise, the use of adjuvant tamoxifen following AC-based regimens did not affect AMH recovery. Both AC-based regimens and CMF significantly compromise ovarian reserve, without a recovery beyond 12 months post-chemotherapy. In contrast, tamoxifen-only treatment does not seem to alter ovarian reserve. These data indicate that the commonly used chemotherapy regimens but not the hormonal therapy compromise future reproductive potential.
Identifiants
pubmed: 32930927
doi: 10.1007/s10549-020-05933-7
pii: 10.1007/s10549-020-05933-7
pmc: PMC7877450
mid: NIHMS1629410
doi:
Substances chimiques
Tamoxifen
094ZI81Y45
Anti-Mullerian Hormone
80497-65-0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
165-173Subventions
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NICHD NIH HHS
ID : R01 HD053112
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001860
Pays : United States
Organisme : Eunice Kennedy Shriver National Institute of Child Health and Human Development
ID : RO1 HD053112
Références
Héry C, Ferlay J, Boniol M, Autier P (2008) Changes in breast cancer incidence and mortality in middle-aged and elderly women in 28 countries with Caucasian majority populations. Ann Oncol 19:1009–1018
doi: 10.1093/annonc/mdm593
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, 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
doi: 10.3322/caac.21492
Bedoschi G, Navarro PA, Oktay K (2016) Chemotherapy-induced damage to ovary: mechanisms and clinical impact. Future Oncol 12:2333–2344
doi: 10.2217/fon-2016-0176
Oktem O, Oktay K (2007) Quantitative assessment of the impact of chemotherapy on ovarian follicle reserve and stromal function. Cancer 110:2222–2229
doi: 10.1002/cncr.23071
Soleimani R, Heytens E, Darzynkiewicz Z, Oktay K (2011) Mechanisms of chemotherapy-induced human ovarian aging: double strand DNA breaks and microvascular compromise. Aging 3:782–793
doi: 10.18632/aging.100363
Tham Y-L, Sexton K, Weiss H, Elledge R, Friedman LC, Kramer R (2007) The rates of chemotherapy-induced amenorrhea in patients treated with adjuvant doxorubicin and cyclophosphamide followed by a taxane. Am J Clin Oncol 30:126–132
doi: 10.1097/01.coc.0000251398.57630.4f
Oktay KH, Bedoschi G, Goldfarb SB, Taylan E, Titus S, Palomaki GE et al (2020) Increased chemotherapy-induced ovarian reserve loss in women with germline BRCA mutations due to oocyte deoxyribonucleic acid double strand break repair deficiency. Fertil Steril 113:1251–1260
doi: 10.1016/j.fertnstert.2020.01.033
Turan V, Oktay K (2020) BRCA-related ATM-mediated DNA double-strand break repair and ovarian aging. Hum Reprod Update 26:43–57
doi: 10.1093/humupd/dmz043
Dunlop CE, Anderson RA (2015) Uses of anti-Mullerian hormone (AMH) measurement before and after cancer treatment in women. Maturitas 80:245–250
doi: 10.1016/j.maturitas.2014.12.005
Durlinger ALL, Visser JA, Themmen APN (2002) Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 124:601–609
doi: 10.1530/rep.0.1240601
Fleming R, Seifer DB, Frattarelli JL, Ruman J (2015) Assessing ovarian response: antral follicle count versus anti-Mullerian hormone. Reprod Biomed Online 31:486–496
doi: 10.1016/j.rbmo.2015.06.015
Hansen KR, Hodnett GM, Knowlton N, Craig LB (2011) Correlation of ovarian reserve tests with histologically determined primordial follicle number. Fertil Steril 95:170–175
doi: 10.1016/j.fertnstert.2010.04.006
Iliodromiti S, Anderson RA, Nelson SM (2015) Technical and performance characteristics of anti-Mullerian hormone and antral follicle count as biomarkers of ovarian response. Hum Reprod Update 21:698–710
doi: 10.1093/humupd/dmu062
Van Rooij IAJ, Broekmans FJM, Scheffer GJ, Looman CWN, Habbema JF, de Jong FH et al (2005) Serum antiMullerian hormone levels best reflect the reproductive decline with age in normal women with proven fertility: a longitudinal study. Fertil Steril 83:979–987
doi: 10.1016/j.fertnstert.2004.11.029
Bentzen JG, Forman JL, Johannsen TH, Pinborg A, Larsen EC, Andersen AN et al (2013) Ovarian antral follicle subclasses and anti-Mullerian hormone during normal reproductive aging. J Clin Endocrinol Metab 98:1602–1611
doi: 10.1210/jc.2012-1829
Jeppesen JV, Anderson RA, Kelsey TW, Christiansen SL, Kristensen SG, Jayaprakasan K et al (2013) Which follicles make the most anti-Müllerian hormone in humans? Evidence for an abrupt decline in AMH production at the time of follicle selection. Mol Hum Reprod 19:519–527
doi: 10.1093/molehr/gat024
Durlinger ALL, Gruijters MJG, Kramer P, Karels B, Kumar TR, Matzuk MM et al (2001) Anti-Mullerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology 142:4891–4899
doi: 10.1210/endo.142.11.8486
Durlinger ALL, Gruijters MJG, Kramer P, Karels B, Ingraham HA, Nachtigal MW et al (2002) Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 140:5789–5796
doi: 10.1210/endo.140.12.7204
Dewailly D, Andersen CY, Balen A, Broekmans F, Dilaver N, Fanchin R et al (2014) The physiology and clinical utility of anti-Mullerian hormone in women. Hum Reprod Update 20:370–385
doi: 10.1093/humupd/dmt062
Riggs R, Kimble T, Oehninger S, Bocca S, Zhao Y, Leader B et al (2011) Anti-Mullerian hormone serum levels predict response to controlled ovarian hyperstimulation but not embryo quality or pregnancy outcome in oocyte donation. Fertil Steril 95:410–412
doi: 10.1016/j.fertnstert.2010.07.1042
Riggs RM, Duran EH, Baker MW, Kimble TD, Hobeika E, Yin L et al (2008) Assessment of ovarian reserve with anti-Mullerian hormone: a comparison of the predictive value of anti-Mullerian hormone, follicle-stimulating hormone, inhibin B, and age. Am J Obstet Gynecol 199(202):e1–8
Broer SL, Eijkemans MJC, Scheffer GJ, van Rooij IA, de Vet A, Themmen AP et al (2011) Anti-Mullerian hormone predicts menopause: a long-term follow-up study in normoovulatory women. J Clin Endocrinol Metab 96:2532–2539
doi: 10.1210/jc.2010-2776
Freeman EW, Sammel MD, Lin H, Gracia CR (2012) Anti-Mullerian hormone as a predictor of time to menopause in late reproductive age women. J Clin Endocrinol Metab 97:1673–1680
doi: 10.1210/jc.2011-3032
Tehrani FR, Solaymani-Dodaran M, Tohidi M, Gohari MR, Azizi F (2013) Modeling age at menopause using serum concentration of anti-mullerian hormone. J Clin Endocrinol Metab 98:729–735
doi: 10.1210/jc.2012-3176
Anderson RA, Cameron DA (2011) Pretreatment serum anti-Mullerian hormone predicts long-term ovarian function and bone mass after chemotherapy for early breast cancer. J Clin Endocrinol Metab 96:1336–1343
doi: 10.1210/jc.2010-2582
Henry NL, Xia R, Schott AF, McConnell D, Banerjee M, Hayes DF (2014) Prediction of postchemotherapy ovarian function using markers of ovarian reserve. Oncologist 19:68–74
doi: 10.1634/theoncologist.2013-0145
Anderson RA, Themmen APN, Al-Qahtani A, Groome NP, Cameron DA (2006) The effects of chemotherapy and long-term gonadotrophin suppression on the ovarian reserve in premenopausal women with breast cancer. Hum Reprod 21:2583–2592
doi: 10.1093/humrep/del201
Lee S, Ozkavukcu S, Heytens E, Moy F, Oktay K (2010) Value of early referral to fertility preservation in young women with breast cancer. J Clin Oncol 28:4683–4686
doi: 10.1200/JCO.2010.30.5748
Su HI, Sammel MD, Green J, Velders L, Stankiewicz C, Matro J et al (2010) Antimullerian hormone and inhibin B are hormone measures of ovarian function in late reproductive-aged breast cancer survivors. Cancer 116:592–599
doi: 10.1002/cncr.24746
Oktay K, Harvey BE, Partridge AH, Quinn GP, Reinecke J, Taylor HS et al (2018) Fertility preservation in patients with cancer: ASCO clinical practice guideline update. J Clin Oncol 36:1994–2001
doi: 10.1200/JCO.2018.78.1914
Lambertini M, Anserini P, Levaggi A, Poggio F, Del Mastro L (2013) Fertility counseling of young breast cancer patients. J Thorac Dis 5:68–80
Fitzmaurice G, Laird N, Ware J (2011) Longitudinal analysis. 2nd edn, Wiley, Hoboken. https://content.sph.harvard.edu/fitzmaur/ala2e/
Partridge AH, Ruddy KJ, Gelber S, Schapira L, Abusief M, Meyer M et al (2010) Ovarian reserve in women who remain premenopausal after chemotherapy for early stage breast cancer. Fertil Steril 94:638–644
doi: 10.1016/j.fertnstert.2009.03.045
Shandley LM, Spencer JB, Fothergill A, Mertens AC, Manatunga A, Paplomata E et al (2017) Impact of tamoxifen therapy on fertility in breast cancer survivors. Fertil Steril 107:243–252.e5
doi: 10.1016/j.fertnstert.2016.10.020
Oktay K, Buyuk E, Davis O, Yermakova I, Veeck L, Rosenwaks Z (2003) Fertility preservation in breast cancer patients: IVF and embryo cryopreservation after ovarian stimulation with tamoxifen. Hum Reprod 18:90–95
doi: 10.1093/humrep/deg045
Yu B, Douglas N, Ferin MJ, Nakhuda GS, Crew K, Lobo RA et al (2010) Changes in markers of ovarian reserve and endocrine function in young women with breast cancer undergoing adjuvant chemotherapy. Cancer 116:2099–2105
pubmed: 20187091
pmcid: 3625425
Trapp E, Steidl J, Rack B, Kupka MS, Andergassen U, Jückstock J et al (2017) Anti-Müllerian hormone (AMH) levels in premenopausal breast cancer patients treated with taxane-based adjuvant chemotherapy: a translational research project of the SUCCESS A study. Breast 35:130–135
doi: 10.1016/j.breast.2017.07.007
Oktay K, Newton H, Mullan J, Gosden RG (1998) Development of human primordial follicles to antral stages in SCID/hpg mice stimulated with follicle stimulating hormone. Hum Reprod 13:1133–1138
doi: 10.1093/humrep/13.5.1133
Bines J, Oleske DM, Cobleigh MA (1996) Ovarian function in premenopausal women treated with adjuvant chemotherapy for breast cancer. J Clin Oncol 14:1718–1729
doi: 10.1200/JCO.1996.14.5.1718
Li F, Turan V, Lierman S, Cuvelier C, De Sutter P, Oktay K (2014) Sphingosine-1-phosphate prevents chemotherapy-induced human primordial follicle death. Hum Reprod 29:107–113
doi: 10.1093/humrep/det391
Plante BJ, Cooper GS, Baird DD, Steiner AZ (2010) The impact of smoking on anti-Mullerian hormone levels in women aged 38 to 50 years. Menopause 17:571–576
pubmed: 20065884
pmcid: 2866786