Journal Article
. 2010 Sep; 28(31):4683-6.
doi: 10.1200/JCO.2010.30.5748.

Value of early referral to fertility preservation in young women with breast cancer

Sanghoon Lee 1 Sinan Ozkavukcu  Elke Heytens  Fred Moy  Kutluk Oktay  
Affiliations
  • PMID: 20876425
  •     13 References
  •     54 citations

Abstract

Purpose: To determine whether early referral to reproductive specialists improves fertility preservation (FP) outcomes and reduces delay in adjuvant treatment in young women with breast cancer.

Patients And Methods: A secondary analysis of a prospective database of patients with breast cancer undergoing ovarian stimulation (OS) for FP by oocyte or embryo cryopreservation was performed.

Results: Of the 154 patients, 93 met the inclusion criteria (mean age, 35.2 ± 4.4 years). Thirty-five of the 93 patients were referred before breast surgery (PreS), and 58 patients were referred after surgery (PostS). The time periods from initial diagnosis (ID) to initiation of OS (42.6 ± 27.7 days for PreS v 71.9 ± 30.7 days for PostS; P < .001) and from ID to initiation of chemotherapy (83.9 ± 24.3 days for PreS v 107.8 ± 42.9 days for PostS; P = .045) were significantly shorter for the PreS group versus the PostS group. Nine (25.7%) of 35 patients in the PreS group versus one (1.7%) of 58 patients in the PostS group were able to undergo two FP cycles (P < .001), resulting in an increased yield of oocytes in the PreS group (18.2% [93 of 511 oocytes] v 0.6% [five of 800 oocytes], respectively; P < .001) and embryos (17.2% [40 of 233 embryos] v 0.6% [two of 357 embryos], respectively; P < .001). Patients who had an oocyte retrieval within 5 weeks of the surgery were able to complete a second cycle within 9 weeks of the surgery.

Conclusion: FP referral before breast surgery enables earlier initiation of cryopreservation cycles and chemotherapy and, when appropriate, multiple FP cycles. Women who can undergo multiple cycles may be at advantage for FP because of a larger number of oocytes or embryos cryopreserved. This is the first study demonstrating the benefit of early FP referral in patients with cancer.

Fertility preservation in female patients.
Murat Sonmezer, Kutluk Oktay.
Hum Reprod Update, 2004 May 14; 10(3). PMID: 15140872
Review.
Fertility preservation and reproduction in cancer patients.
Ethics Committee of the American Society for Reproductive Medicine.
Fertil Steril, 2005 Jun 14; 83(6). PMID: 15950628
Fertility preservation in breast cancer patients: a prospective controlled comparison of ovarian stimulation with tamoxifen and letrozole for embryo cryopreservation.
Kutluk Oktay, Erkan Buyuk, +2 authors, Zev Rosenwaks.
J Clin Oncol, 2005 Apr 13; 23(19). PMID: 15824416
Does timing of adjuvant chemotherapy influence the prognosis after early breast cancer? Results of the Danish Breast Cancer Cooperative Group (DBCG).
S Cold, M Düring, +2 authors, S Møller.
Br J Cancer, 2005 Sep 02; 93(6). PMID: 16136052    Free PMC article.
Fertility preservation in young women undergoing breast cancer therapy.
Murat Sonmezer, Kutluk Oktay.
Oncologist, 2006 May 25; 11(5). PMID: 16720842
Review.
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.
Efficiency of oocyte cryopreservation: a meta-analysis.
Kutluk Oktay, Aylin Pelin Cil, Heejung Bang.
Fertil Steril, 2006 Jul 05; 86(1). PMID: 16818031
Letrozole reduces estrogen and gonadotropin exposure in women with breast cancer undergoing ovarian stimulation before chemotherapy.
Kutluk Oktay, Ariel Hourvitz, +4 authors, Heejung Bang.
J Clin Endocrinol Metab, 2006 Aug 03; 91(10). PMID: 16882752
Impact on survival of time from definitive surgery to initiation of adjuvant chemotherapy for early-stage breast cancer.
Caroline Lohrisch, Charles Paltiel, +4 authors, Ivo A Olivotto.
J Clin Oncol, 2006 Oct 04; 24(30). PMID: 17015884
Safety of fertility preservation by ovarian stimulation with letrozole and gonadotropins in patients with breast cancer: a prospective controlled study.
Amr A Azim, Maria Costantini-Ferrando, Kutluk Oktay.
J Clin Oncol, 2008 May 30; 26(16). PMID: 18509175
Highly Cited.
Pilot survey of oncologists regarding treatment-related infertility and fertility preservation in female cancer patients.
Eric J Forman, Carey K Anders, Millie A Behera.
J Reprod Med, 2009 May 15; 54(4). PMID: 19438160    Free PMC article.
Physician referral for fertility preservation in oncology patients: a national study of practice behaviors.
Gwendolyn P Quinn, Susan T Vadaparampil, +5 authors, Terrance L Albrecht.
J Clin Oncol, 2009 Oct 15; 27(35). PMID: 19826115
Highly Cited.
Association of BRCA1 mutations with occult primary ovarian insufficiency: a possible explanation for the link between infertility and breast/ovarian cancer risks.
Kutluk Oktay, Ja Yeon Kim, David Barad, Samir N Babayev.
J Clin Oncol, 2009 Dec 10; 28(2). PMID: 19996028    Free PMC article.
Highly Cited.
Fertility: The importance of early referral to fertility preservation.
Lisa Richards.
Nat Rev Clin Oncol, 2011 Jan 11; 8(1). PMID: 21218527
Determinants of access to fertility preservation in women with breast cancer.
Sanghoon Lee, Elke Heytens, +2 authors, Kutluk Oktay.
Fertil Steril, 2011 Mar 05; 95(6). PMID: 21371704    Free PMC article.
Which patients pursue fertility preservation treatments? A multicenter analysis of the predictors of fertility preservation in women with breast cancer.
Jayeon Kim, Kutluk Oktay, +3 authors, Jennifer E Mersereau.
Fertil Steril, 2012 Jan 10; 97(3). PMID: 22222194    Free PMC article.
Breast cancer and fertility.
Jennifer K Litton.
Curr Treat Options Oncol, 2012 Mar 08; 13(2). PMID: 22396154
Review.
Fertility preservation in women undergoing treatment for breast cancer in the UK: a questionnaire study.
Judy W King, Melanie C Davies, +2 authors, Alison L Jones.
Oncologist, 2012 Jun 19; 17(7). PMID: 22707514    Free PMC article.
Does higher starting dose of FSH stimulation with letrozole improve fertility preservation outcomes in women with breast cancer?
Sanghoon Lee, Kutluk Oktay.
Fertil Steril, 2012 Jul 10; 98(4). PMID: 22771027    Free PMC article.
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.
Fertility preservation and pregnancy in women with and without BRCA mutation-positive breast cancer.
Kenny A Rodriguez-Wallberg, Kutluk Oktay.
Oncologist, 2012 Sep 26; 17(11). PMID: 23006497    Free PMC article.
Current approach to fertility preservation by embryo cryopreservation.
Giuliano Bedoschi, Kutluk Oktay.
Fertil Steril, 2013 Mar 29; 99(6). PMID: 23535505    Free PMC article.
Review.
Women's experiences with information provision and deciding about fertility preservation in the Netherlands: 'satisfaction in general, but unmet needs'.
Mirjam M Garvelink, Moniek M ter Kuile, +5 authors, Anne M Stiggelbout.
Health Expect, 2013 May 08; 18(5). PMID: 23647741    Free PMC article.
Breast cancer in the young: role of the geneticist.
Ashley H Woodson, Jessica L Profato, Kimberly I Muse, Jennifer K Litton.
J Thorac Dis, 2013 Jul 03; 5 Suppl 1. PMID: 23819023    Free PMC article.
Safety and feasibility of performing two consecutive ovarian stimulation cycles with the use of letrozole-gonadotropin protocol for fertility preservation in breast cancer patients.
Volkan Turan, Giuliano Bedoschi, Fred Moy, Kutluk Oktay.
Fertil Steril, 2013 Sep 24; 100(6). PMID: 24055050    Free PMC article.
Oncofertility in Canada: an overview of Canadian practice and suggested action plan.
R Ronn, H E G Holzer.
Curr Oncol, 2013 Oct 25; 20(5). PMID: 24155643    Free PMC article.
Triggering final oocyte maturation with gonadotropin-releasing hormone agonist (GnRHa) versus human chorionic gonadotropin (hCG) in breast cancer patients undergoing fertility preservation: an extended experience.
Jhansi Reddy, Volkan Turan, +2 authors, Kutluk Oktay.
J Assist Reprod Genet, 2014 May 24; 31(7). PMID: 24854484    Free PMC article.
Estimates of young breast cancer survivors at risk for infertility in the U.S.
Katrina F Trivers, Aliza K Fink, +4 authors, Lori A Pollack.
Oncologist, 2014 Jun 22; 19(8). PMID: 24951610    Free PMC article.
Fertility issues of breast cancer survivors.
Hollis McClellan Misiewicz.
J Adv Pract Oncol, 2012 Sep 01; 3(5). PMID: 25031958    Free PMC article.
Review.
Preserving fertility in patients undergoing treatment for breast cancer: current perspectives.
Rebecca Moffat, Uwe Güth.
Breast Cancer (Dove Med Press), 2014 Aug 13; 6. PMID: 25114587    Free PMC article.
Review.
A review of breast cancer survivorship issues from survivors' perspectives.
Jihyoung Cho, So-Youn Jung, +9 authors, Min Hyuk Lee.
J Breast Cancer, 2014 Oct 17; 17(3). PMID: 25320616    Free PMC article.
Review.
Early referral makes the decision-making about fertility preservation easier: a pilot survey study of young female cancer survivors.
Jayeon Kim, Jennifer E Mersereau.
Support Care Cancer, 2014 Nov 26; 23(6). PMID: 25421445
Challenges and considerations in optimizing ovarian stimulation protocols in oncofertility patients.
Kathryn Coyne, MacKenzie Purdy, +3 authors, Leslie A Appiah.
Front Public Health, 2014 Dec 30; 2. PMID: 25538933    Free PMC article.
Review.
Occurrence and recall rates of fertility discussions with young breast cancer patients.
Rahul Banerjee, Ekaterini Tsiapali.
Support Care Cancer, 2015 May 15; 24(1). PMID: 25967235
Fertility preservation in young cancer patients--too little, too late?
Helen Louise Robbins, Arooba Zahoor, Kevin Jones.
Support Care Cancer, 2015 Aug 19; 23(12). PMID: 26279146
Fertility preservation in reproductive-age women facing gonadotoxic treatments.
J Roberts, R Ronn, N Tallon, H Holzer.
Curr Oncol, 2015 Aug 25; 22(4). PMID: 26300680    Free PMC article.
Factors associated with the receipt of fertility preservation services along the decision-making pathway in young Canadian female cancer patients.
Samantha Yee.
J Assist Reprod Genet, 2015 Nov 13; 33(2). PMID: 26560157    Free PMC article.
Long-Term Safety of Letrozole and Gonadotropin Stimulation for Fertility Preservation in Women With Breast Cancer.
Jayeon Kim, Volkan Turan, Kutluk Oktay.
J Clin Endocrinol Metab, 2016 Jan 12; 101(4). PMID: 26751194    Free PMC article.
Fertility Preservation for the Young Breast Cancer Patient.
Shari B Goldfarb, Sabrina A Kamer, +6 authors, Mary L Gemignani.
Ann Surg Oncol, 2016 Jan 23; 23(5). PMID: 26790670    Free PMC article.
Fertility Preservation: A Key Survivorship Issue for Young Women with Cancer.
Ana Milena Angarita, Cynae A Johnson, Amanda Nickles Fader, Mindy S Christianson.
Front Oncol, 2016 May 21; 6. PMID: 27200291    Free PMC article.
Review.
Cryopreservation of in vitro matured oocytes after ex vivo oocyte retrieval from gynecologic cancer patients undergoing radical surgery.
Chan Woo Park, Sun Hee Lee, +4 authors, Tae Jin Kim.
Clin Exp Reprod Med, 2016 Jul 01; 43(2). PMID: 27358831    Free PMC article.
Which female cancer patients fail to receive fertility counseling before treatment in the state of Georgia?
Helen B Chin, Penelope P Howards, +2 authors, Jessica B Spencer.
Fertil Steril, 2016 Sep 30; 106(7). PMID: 27678034    Free PMC article.
Reproductive Decision-Making in Women with BRCA1/2 Mutations.
Jessica L Chan, Lauren N C Johnson, +4 authors, Clarisa R Gracia.
J Genet Couns, 2016 Nov 01; 26(3). PMID: 27796678    Free PMC article.
On-Site Fertility Preservation Services for Adolescents and Young Adults in a Comprehensive Cancer Center.
Mary Peavey, Sara Arian, +3 authors, Terri Woodard.
J Adolesc Young Adult Oncol, 2016 Nov 16; 6(2). PMID: 27845854    Free PMC article.
Management of Potential Long-Term Toxicities in Breast Cancer Patients.
C C O'Sullivan, K J Ruddy.
Curr Breast Cancer Rep, 2017 May 16; 8(4). PMID: 28503254    Free PMC article.
Current state and controversies in fertility preservation in women with breast cancer.
Enes Taylan, Kutluk H Oktay.
World J Clin Oncol, 2017 Jun 24; 8(3). PMID: 28638793    Free PMC article.
Review.
Oncology Physicians' Perspectives on Practices and Barriers to Fertility Preservation and the Feasibility of a Prospective Study of Pregnancy After Breast Cancer.
Shoshana M Rosenberg, Shari Gelber, +4 authors, Ann H Partridge.
J Adolesc Young Adult Oncol, 2017 Jul 08; 6(3). PMID: 28686476    Free PMC article.
Cancer survivors of gynecologic malignancies are at risk for decreased opportunity for fertility preservation.
Wael H Salem, Joe M Letourneau, +3 authors, Mitchell P Rosen.
Contracept Reprod Med, 2017 Dec 05; 2. PMID: 29201417    Free PMC article.
Fertility preservation for patients with breast cancer: The Korean Society for Fertility Preservation clinical guidelines.
Hoon Kim, Seul Ki Kim, +3 authors, Seok Hyun Kim.
Clin Exp Reprod Med, 2018 Jan 30; 44(4). PMID: 29376014    Free PMC article.
Review.
Successful in Vitro Fertilization and Embryo Transfer after Transplantation of Cryopreserved Ovarian Tissue: Report of the First Korean Case.
Jung Ryeol Lee, Dayong Lee, +5 authors, Seok Hyun Kim.
J Korean Med Sci, 2018 May 22; 33(21). PMID: 29780295    Free PMC article.
Fertility preservation in pediatric and young adult female cancer patients.
Hashin Kim, Hoon Kim, Seung-Yup Ku.
Ann Pediatr Endocrinol Metab, 2018 Jul 05; 23(2). PMID: 29969877    Free PMC article.
Ovarian tissue cryopreservation and transplantation in patients with cancer.
Sooyoung Kim, Younji Lee, Sanghoon Lee, Tak Kim.
Obstet Gynecol Sci, 2018 Jul 19; 61(4). PMID: 30018897    Free PMC article.
Review.

;. PMID: 30241266
Fertility preservation in BRCA mutation carriers-efficacy and safety issues: a review.
Xiaofu Zhang, Jingxin Niu, +3 authors, Jing Qu.
Reprod Biol Endocrinol, 2020 Feb 20; 18(1). PMID: 32070378    Free PMC article.
Review.
Patterns of Referral for Fertility Preservation Among Female Adolescents and Young Adults with Breast Cancer: A Population-Based Study.
Ann Korkidakis, Katherine Lajkosz, +2 authors, Maria P Velez.
J Adolesc Young Adult Oncol, 2019 Jan 25; 8(2). PMID: 30676852    Free PMC article.
Is Fertility Preservation Feasible and Safe With Neoadjuvant Therapy for Breast Cancer?
Avner Hershlag, Christine Mullin, Sara L Bristow.
JCO Glob Oncol, 2020 Apr 08; 6. PMID: 32259161    Free PMC article.
Ovarian stimulation is a safe and effective fertility preservation option in the adolescent and young adult population.
Sharrόn L Manuel, Molly B Moravek, +4 authors, Mary Ellen Pavone.
J Assist Reprod Genet, 2019 Dec 13; 37(3). PMID: 31828481    Free PMC article.
Issues with Fertility in Young Women with Breast Cancer.
Nicole Christian, Mary L Gemignani.
Curr Oncol Rep, 2019 May 18; 21(7). PMID: 31098718
Review.
Does Use of Neoadjuvant Chemotherapy Affect the Decision to Pursue Fertility Preservation Options in Young Women with Breast Cancer?
Angelena Crown, Shirin Muhsen, +4 authors, Mary L Gemignani.
Ann Surg Oncol, 2020 Aug 09; 27(12). PMID: 32767225    Free PMC article.
Advances in the Treatment and Prevention of Chemotherapy-Induced Ovarian Toxicity.
Hyun-Woong Cho, Sanghoon Lee, +5 authors, Tak Kim.
Int J Mol Sci, 2020 Oct 25; 21(20). PMID: 33096794    Free PMC article.
Review.
The current fertility preservation consultation model: are we adequately informing cancer patients of their options?
Ursula Balthazar, Allison M Deal, +3 authors, Jennifer E Mersereau.
Hum Reprod, 2012 Jun 08; 27(8). PMID: 22674206    Free PMC article.
Factors associated with treatment delay in women with primary breast cancer who were referred to reproductive specialists.
Atsuko Kitano, Chikako Shimizu, +4 authors, Sachiko Ohde.
ESMO Open, 2019 Apr 10; 4(2). PMID: 30962960    Free PMC article.
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.
FERTILITY PRESERVATION IN YOUNG WOMEN WITH EARLY-STAGE BREAST CANCER.
Petra Vuković, Miro Kasum, +5 authors, Ermin Čehić.
Acta Clin Croat, 2019 Aug 01; 58(1). PMID: 31363337    Free PMC article.
Review.
Changes in telomere length and senescence markers during human ovarian tissue cryopreservation.
Boram Kim, Ki-Jin Ryu, Sanghoon Lee, Tak Kim.
Sci Rep, 2021 Jan 28; 11(1). PMID: 33500500    Free PMC article.
Impact of adjuvant chemotherapy or tamoxifen-alone on the ovarian reserve of young women with breast cancer.
Shari B Goldfarb, Volkan Turan, +7 authors, Kutluk H Oktay.
Breast Cancer Res Treat, 2020 Sep 16; 185(1). PMID: 32930927    Free PMC article.
Current and Future Perspectives for Improving Ovarian Tissue Cryopreservation and Transplantation Outcomes for Cancer Patients.
Sanghoon Lee, Sinan Ozkavukcu, Seung-Yup Ku.
Reprod Sci, 2021 Apr 02; 28(6). PMID: 33791995    Free PMC article.
Review.