Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 8/2016

01-08-2016 | Review

Ovarian stimulation in the luteal phase: systematic review and meta-analysis

Authors: C. E. Boots, M. Meister, A. R. Cooper, A. Hardi, E. S. Jungheim

Published in: Journal of Assisted Reproduction and Genetics | Issue 8/2016

Login to get access

Abstract

Purpose

The purpose of this study was to evaluate whether outcomes are different if controlled ovarian stimulation (COS) is started in the luteal phase rather than the follicular phase.

Methods

A systematic review and meta-analysis was performed. Sixteen studies were included in the qualitative analysis, and eight studies with a total of 338 women were included in the quantitative analysis.

Results

Cycles initiated in the luteal phase were slightly longer (WMD 1.1 days, 95 % CI 0.39–1.9) and utilized more total gonadotropins (WMD 817 IU, 95 % CI 489–1144). However, no differences were noted in peak estradiol levels (WMD −411 pg/ml, 95 % CI −906–84.7) or in the total number of oocytes retrieved (WMD 0.52 oocytes, 95 % CI −0.74–1.7). There were slightly more mature oocytes retrieved in the luteal phase (WMD 0.77 oocytes, 95 % CI 0.21–1.3), and fertilization rates were significantly higher (WMD 10 %, 95 % CI 0.03–0.18). While only three studies reported pregnancy outcomes, no difference was noted in the FET pregnancy rates after COS in the luteal versus follicular phase (RR 0.95, 95 % CI 0.56–1.7).
A post hoc power analysis revealed that a sample of this size was sufficient to detect a clinically meaningful difference of 2 oocytes retrieved with 93 % power.

Conclusion

Although initiating COS in the luteal phase requires a longer stimulation and a higher dose of total gonadotropin, these differences are not clinically significant. Furthermore, COS initiated in the luteal phase does not compromise the quantity or quality of oocytes retrieved compared to outcomes of traditional stimulation in the follicular phase.
Appendix
Available only for authorised users
Literature
1.
go back to reference Howlader N, Noone A, Krapcho M, Garshell J, Miller D, Altekruse S, et al. SEER Cancer Statistics Review, 1975–2012, National Cancer Institute. Bethesda, MD, http://seer.cancer.gov/csr/1975_2012/, based on November 2014 SEER data submission posted to the SEER website. 2015. Howlader N, Noone A, Krapcho M, Garshell J, Miller D, Altekruse S, et al. SEER Cancer Statistics Review, 1975–2012, National Cancer Institute. Bethesda, MD, http://​seer.​cancer.​gov/​csr/​1975_​2012/​, based on November 2014 SEER data submission posted to the SEER website. 2015.
2.
go back to reference Lee SJ, Schover LR, Partridge AH, Patrizio P, Wallace WH, Hagerty K, et al. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol. 2006;24(18):2917–31.CrossRefPubMed Lee SJ, Schover LR, Partridge AH, Patrizio P, Wallace WH, Hagerty K, et al. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol. 2006;24(18):2917–31.CrossRefPubMed
3.
go back to reference Loren AW, Mangu PB, Beck LN, Brennan L, Magdalinski AJ, Partridge AH, et al. Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2013;31(19):2500–10.CrossRefPubMed Loren AW, Mangu PB, Beck LN, Brennan L, Magdalinski AJ, Partridge AH, et al. Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2013;31(19):2500–10.CrossRefPubMed
4.
go back to reference Fertility preservation in patients undergoing gonadotoxic therapy or gonadectomy: a committee opinion. Fertil Steril 2013;100(5):1214–23. Fertility preservation in patients undergoing gonadotoxic therapy or gonadectomy: a committee opinion. Fertil Steril 2013;100(5):1214–23.
5.
6.
go back to reference Baerwald AR, Adams GP, Pierson RA. A new model for ovarian follicular development during the human menstrual cycle. Fertil Steril. 2003;80(1):116–22.CrossRefPubMed Baerwald AR, Adams GP, Pierson RA. A new model for ovarian follicular development during the human menstrual cycle. Fertil Steril. 2003;80(1):116–22.CrossRefPubMed
7.
go back to reference von Wolff M, Thaler CJ, Frambach T, Zeeb C, Lawrenz B, Popovici RM, et al. Ovarian stimulation to cryopreserve fertilized oocytes in cancer patients can be started in the luteal phase. Fertil Steril. 2009;92(4):1360–5.CrossRef von Wolff M, Thaler CJ, Frambach T, Zeeb C, Lawrenz B, Popovici RM, et al. Ovarian stimulation to cryopreserve fertilized oocytes in cancer patients can be started in the luteal phase. Fertil Steril. 2009;92(4):1360–5.CrossRef
8.
go back to reference Sonmezer M, Turkcuoglu I, Coskun U, Oktay K. Random-start controlled ovarian hyperstimulation for emergency fertility preservation in letrozole cycles. Fertil Steril 2011;95(6). Sonmezer M, Turkcuoglu I, Coskun U, Oktay K. Random-start controlled ovarian hyperstimulation for emergency fertility preservation in letrozole cycles. Fertil Steril 2011;95(6).
9.
go back to reference Nayak SR, Wakim AN. Random-start gonadotropin-releasing hormone (GnRH) antagonist-treated cycles with GnRH agonist trigger for fertility preservation. Fertil Steril. 2011;96(1):e51–4.CrossRefPubMed Nayak SR, Wakim AN. Random-start gonadotropin-releasing hormone (GnRH) antagonist-treated cycles with GnRH agonist trigger for fertility preservation. Fertil Steril. 2011;96(1):e51–4.CrossRefPubMed
10.
11.
go back to reference Cakmak H, Katz A, Cedars MI, Rosen MP. Effective method for emergency fertility preservation: random-start controlled ovarian stimulation. Fertil Steril. 2013;100(6):1673–80.CrossRefPubMed Cakmak H, Katz A, Cedars MI, Rosen MP. Effective method for emergency fertility preservation: random-start controlled ovarian stimulation. Fertil Steril. 2013;100(6):1673–80.CrossRefPubMed
12.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–9.CrossRefPubMed Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–9.CrossRefPubMed
13.
go back to reference Higgins J, Green S (ed). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.cochrane-handbook.org. Higgins J, Green S (ed). Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from www.​cochrane-handbook.​org.
14.
15.
go back to reference Higgins J, Thompson S. Quantifying heterogeneity in a meta‐analysis. Stat Med. 2002;21:1539–58.CrossRefPubMed Higgins J, Thompson S. Quantifying heterogeneity in a meta‐analysis. Stat Med. 2002;21:1539–58.CrossRefPubMed
16.
go back to reference Hussein G, Lood M. Random-start IVF treatment: an emergent fertility preservation technique between cytotoxic treatment courses and stem-cell transplantation in acute myelocytic leukemia. Middle East Fertil Soc J 2015;20:297–300. Hussein G, Lood M. Random-start IVF treatment: an emergent fertility preservation technique between cytotoxic treatment courses and stem-cell transplantation in acute myelocytic leukemia. Middle East Fertil Soc J 2015;20:297–300.
17.
go back to reference Friedman BE, Pao S, Westphal LM, Lathi RB. Oocyte retrieval following continued stimulation five days beyond ovulation yields live birth after frozen embryo transfer. J Assist Reprod Genet. 2012;29(5):433–5.CrossRefPubMedPubMedCentral Friedman BE, Pao S, Westphal LM, Lathi RB. Oocyte retrieval following continued stimulation five days beyond ovulation yields live birth after frozen embryo transfer. J Assist Reprod Genet. 2012;29(5):433–5.CrossRefPubMedPubMedCentral
18.
go back to reference Friedman BE, Pao S, Westphal LM, Lathi RB. Successful oocyte retrieval and fertilization following continued stimulation 5 days beyond ovulation. Fertil Steril. 2011;95(4):S13.CrossRef Friedman BE, Pao S, Westphal LM, Lathi RB. Successful oocyte retrieval and fertilization following continued stimulation 5 days beyond ovulation. Fertil Steril. 2011;95(4):S13.CrossRef
19.
go back to reference Friedler S, Koc O, Gidoni Y, Raziel A, Ron-El R. Ovarian response to stimulation for fertility preservation in women with malignant disease: a systematic review and meta-analysis. Fertil Steril. 2012;97(1):125–33.CrossRefPubMed Friedler S, Koc O, Gidoni Y, Raziel A, Ron-El R. Ovarian response to stimulation for fertility preservation in women with malignant disease: a systematic review and meta-analysis. Fertil Steril. 2012;97(1):125–33.CrossRefPubMed
20.
go back to reference Huober-Zeeb C, Lawrenz B, Popovici RM, Strowitzki T, Germeyer A, Stute P, et al. Improving fertility preservation in cancer: ovarian tissue cryobanking followed by ovarian stimulation can be efficiently combined. Fertil Steril. 2011;95(1):342–4.CrossRefPubMed Huober-Zeeb C, Lawrenz B, Popovici RM, Strowitzki T, Germeyer A, Stute P, et al. Improving fertility preservation in cancer: ovarian tissue cryobanking followed by ovarian stimulation can be efficiently combined. Fertil Steril. 2011;95(1):342–4.CrossRefPubMed
21.
go back to reference Lawrenz B, Jauckus J, Kupka MS, Strowitzki T, von Wolff M. Fertility preservation in >1,000 patients: patient’s characteristics, spectrum, efficacy and risks of applied preservation techniques. Arch Gynecol Obstet. 2011;283(3):651–6.CrossRefPubMed Lawrenz B, Jauckus J, Kupka MS, Strowitzki T, von Wolff M. Fertility preservation in >1,000 patients: patient’s characteristics, spectrum, efficacy and risks of applied preservation techniques. Arch Gynecol Obstet. 2011;283(3):651–6.CrossRefPubMed
22.
go back to reference Lawrenz B, Neunhoeffer E, Henes M, Lessmann-Bechle S, Kramer B, Fehm T. Management of fertility preservation in young breast cancer patients in a large breast cancer centre. Arch Gynecol Obstet. 2010;282(5):547–51.CrossRefPubMed Lawrenz B, Neunhoeffer E, Henes M, Lessmann-Bechle S, Kramer B, Fehm T. Management of fertility preservation in young breast cancer patients in a large breast cancer centre. Arch Gynecol Obstet. 2010;282(5):547–51.CrossRefPubMed
23.
go back to reference El-Toukhy T, Taranissi M. Which is more counterproductive: a brief delay or “start anyway”? Hum Reprod Oxf Engl. 2006;21(9):2456–7. author reply 2457–8.CrossRef El-Toukhy T, Taranissi M. Which is more counterproductive: a brief delay or “start anyway”? Hum Reprod Oxf Engl. 2006;21(9):2456–7. author reply 2457–8.CrossRef
24.
go back to reference von Wolff M, Donnez J, Hovatta O, Keros V, Maltaris T, Montag M, et al. Cryopreservation and autotransplantation of human ovarian tissue prior to cytotoxic therapy—a technique in its infancy but already successful in fertility preservation. Eur J Cancer Oxf Engl 1990. 2009;45(9):1547–53. von Wolff M, Donnez J, Hovatta O, Keros V, Maltaris T, Montag M, et al. Cryopreservation and autotransplantation of human ovarian tissue prior to cytotoxic therapy—a technique in its infancy but already successful in fertility preservation. Eur J Cancer Oxf Engl 1990. 2009;45(9):1547–53.
25.
go back to reference Shalom-Paz E, Holzer HEG. Fertility preservation for cancer patients. Current Options Minerva Ginecol. 2011;63(6):517–30.PubMed Shalom-Paz E, Holzer HEG. Fertility preservation for cancer patients. Current Options Minerva Ginecol. 2011;63(6):517–30.PubMed
26.
go back to reference von Wolff M, Zeeb C, Lawrenz B, Germeyer A, Neunhoeffer E, Strowitzki T. Cryopreservation of ovarian tissue and cryopreservation of oocytes can be efficiently combined and performed within 2 weeks before chemotherapy. Mol Hum Reprod. 2009;24:i157.CrossRef von Wolff M, Zeeb C, Lawrenz B, Germeyer A, Neunhoeffer E, Strowitzki T. Cryopreservation of ovarian tissue and cryopreservation of oocytes can be efficiently combined and performed within 2 weeks before chemotherapy. Mol Hum Reprod. 2009;24:i157.CrossRef
27.
go back to reference Kuang Y, Chen Q, Hong Q, Lyu Q, Ai A, Fu Y, et al. Double stimulations during the follicular and luteal phases of poor responders in IVF/ICSI programmes (Shanghai protocol). Reprod Biomed Online. 2014;29(6):684–91.CrossRefPubMed Kuang Y, Chen Q, Hong Q, Lyu Q, Ai A, Fu Y, et al. Double stimulations during the follicular and luteal phases of poor responders in IVF/ICSI programmes (Shanghai protocol). Reprod Biomed Online. 2014;29(6):684–91.CrossRefPubMed
28.
go back to reference Kuang Y, Hong Q, Chen Q, Lyu Q, Ai A, Fu Y, et al. 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. 2014;101(1):105–11.CrossRefPubMed Kuang Y, Hong Q, Chen Q, Lyu Q, Ai A, Fu Y, et al. 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. 2014;101(1):105–11.CrossRefPubMed
29.
go back to reference Martinez F, Clua E, Devesa M, Rodriguez I, Arroyo G, Gonzalez C, et al. 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. 2014;102(5):1307–11.CrossRefPubMed Martinez F, Clua E, Devesa M, Rodriguez I, Arroyo G, Gonzalez C, et al. 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. 2014;102(5):1307–11.CrossRefPubMed
30.
go back to reference Kim JH, Kim SK, Lee HJ, Lee JR, Jee BC, Suh CS, et al. Efficacy of random-start controlled ovarian stimulation in cancer patients. J Korean Med Sci. 2015;30(3):290.CrossRefPubMedPubMedCentral Kim JH, Kim SK, Lee HJ, Lee JR, Jee BC, Suh CS, et al. Efficacy of random-start controlled ovarian stimulation in cancer patients. J Korean Med Sci. 2015;30(3):290.CrossRefPubMedPubMedCentral
31.
go back to reference Rashidi BH, Tehrani ES, Ghaffari F. Ovarian stimulation for emergency fertility preservation in cancer patients: a case series study. Gynecol Oncol Rep. 2014;10:19–21.CrossRefPubMedPubMedCentral Rashidi BH, Tehrani ES, Ghaffari F. Ovarian stimulation for emergency fertility preservation in cancer patients: a case series study. Gynecol Oncol Rep. 2014;10:19–21.CrossRefPubMedPubMedCentral
32.
go back to reference Suikkari AM, Tulppala M, Tuuri T, Hovatta O, Barnes F. Luteal phase start of low-dose FSH priming of follicles results in an efficient recovery, maturation and fertilization of immature human oocytes. Hum Reprod Oxf Engl. 2000;15(4):747–51.CrossRef Suikkari AM, Tulppala M, Tuuri T, Hovatta O, Barnes F. Luteal phase start of low-dose FSH priming of follicles results in an efficient recovery, maturation and fertilization of immature human oocytes. Hum Reprod Oxf Engl. 2000;15(4):747–51.CrossRef
33.
go back to reference Buendgen NK, Schultze-Mosgau A, Cordes T, Diedrich K, Griesinger G. Initiation of ovarian stimulation independent of the menstrual cycle: a case-control study. Arch Gynecol Obstet. 2013;288(4):901–4.CrossRefPubMed Buendgen NK, Schultze-Mosgau A, Cordes T, Diedrich K, Griesinger G. Initiation of ovarian stimulation independent of the menstrual cycle: a case-control study. Arch Gynecol Obstet. 2013;288(4):901–4.CrossRefPubMed
34.
go back to reference Maman E, Meirow D, Brengauz M, Raanani H, Dor J, Hourvitz A. Luteal phase oocyte retrieval and in vitro maturation is an optional procedure for urgent fertility preservation. Fertil Steril. 2011;95(1):64–7.CrossRefPubMed Maman E, Meirow D, Brengauz M, Raanani H, Dor J, Hourvitz A. Luteal phase oocyte retrieval and in vitro maturation is an optional procedure for urgent fertility preservation. Fertil Steril. 2011;95(1):64–7.CrossRefPubMed
35.
go back to reference Bedoschi GM, de Albuquerque FO, Ferriani RA, Navarro PA. Ovarian stimulation during the luteal phase for fertility preservation of cancer patients: case reports and review of the literature. J Assist Reprod Genet. 2010;27(8):491–4.CrossRefPubMedPubMedCentral Bedoschi GM, de Albuquerque FO, Ferriani RA, Navarro PA. Ovarian stimulation during the luteal phase for fertility preservation of cancer patients: case reports and review of the literature. J Assist Reprod Genet. 2010;27(8):491–4.CrossRefPubMedPubMedCentral
36.
go back to reference Dittrich R, Lotz L, Mueller A, Hoffmann I, Wachter DL, Amann KU, et al. Oncofertility: combination of ovarian stimulation with subsequent ovarian tissue extraction on the day of oocyte retrieval. Reprod Biol Endocrinol. 2013;11:19.CrossRefPubMedPubMedCentral Dittrich R, Lotz L, Mueller A, Hoffmann I, Wachter DL, Amann KU, et al. Oncofertility: combination of ovarian stimulation with subsequent ovarian tissue extraction on the day of oocyte retrieval. Reprod Biol Endocrinol. 2013;11:19.CrossRefPubMedPubMedCentral
37.
go back to reference Keskin U, Ercan CM, Yilmaz A, Babacan A, Korkmaz C, Duru NK, et al. Random-start controlled ovarian hyperstimulation with letrozole for fertility preservation in cancer patients: case series and review of literature. J Pak Med Assoc. 2014;64(7):830–2.PubMed Keskin U, Ercan CM, Yilmaz A, Babacan A, Korkmaz C, Duru NK, et al. Random-start controlled ovarian hyperstimulation with letrozole for fertility preservation in cancer patients: case series and review of literature. J Pak Med Assoc. 2014;64(7):830–2.PubMed
38.
go back to reference Schuffner A, Skroch R, Garbelini M, Neto J, Peixoto A, da Rosa V. Ovarian stimulation in the follicular, late follicular and luteal phases: an ideal protocol for the preservation of fertility? J Bras Reprod Assist. 2012;16:91–3. Schuffner A, Skroch R, Garbelini M, Neto J, Peixoto A, da Rosa V. Ovarian stimulation in the follicular, late follicular and luteal phases: an ideal protocol for the preservation of fertility? J Bras Reprod Assist. 2012;16:91–3.
39.
go back to reference Reynolds KA, Grindler NM, Rhee JS, Cooper AR, Ratts VS, Carson KR, et al. Variability in the practice of fertility preservation for patients with cancer. PLoS One. 2015;10(5):e0127335.CrossRefPubMedPubMedCentral Reynolds KA, Grindler NM, Rhee JS, Cooper AR, Ratts VS, Carson KR, et al. Variability in the practice of fertility preservation for patients with cancer. PLoS One. 2015;10(5):e0127335.CrossRefPubMedPubMedCentral
Metadata
Title
Ovarian stimulation in the luteal phase: systematic review and meta-analysis
Authors
C. E. Boots
M. Meister
A. R. Cooper
A. Hardi
E. S. Jungheim
Publication date
01-08-2016
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 8/2016
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-016-0721-5

Other articles of this Issue 8/2016

Journal of Assisted Reproduction and Genetics 8/2016 Go to the issue