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

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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.

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Acknowledgments

C.E.B. received support from the National Research Training Program in Reproductive Medicine sponsored by the National Institute of Health (T32 HD040135-13) and the Scientific Advisory Board of Vivere Health. E.S.J. received support from the Women’s Reproductive Health Research (WRHR) Program sponsored by the National Institute of Health (K12 HD063086), the Institute of Clinical and Translational Sciences (ICTS) at Washington University (UL1 TR000448), the Barnes Jewish Hospital Foundation, and the March of Dimes. A.R.C also received funding from the WRHR and ICTS programs.

Author information

Authors and Affiliations

  1. Obstetrics & Gynecology, Washington University, 4444 Forest Park, Suite 3100, St. Louis, MO, 63108, USA

    C. E. Boots, M. Meister, A. R. Cooper & E. S. Jungheim

  2. Washington University, 660 Euclid Avenue, St. Louis, MO, 63110, USA

    A. Hardi

Authors
  1. C. E. Boots
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  2. M. Meister
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  3. A. R. Cooper
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Corresponding author

Correspondence to C. E. Boots.

Ethics declarations

Institutional review board approval was obtained from Washington University prior to the chart review and data extraction.

Conflict of Interest

The authors declare that they have no conflicts of interest.

Additional information

Capsule

Ovarian stimulation may safely and effectively be initiated in the luteal phase without compromising oocyte number or quality.

Appendix: Systematic review search strategies

Appendix: Systematic review search strategies

PubMed

(“Neoplasms” [Mesh] OR “neoplasm” OR “neoplasms” OR “cancer” OR “cancers” OR “neoplasia” OR “neoplasias” OR “carcinoma” OR “sarcoma” OR “sarcomas” OR “neoplastic disease”) AND (“Fertilization in Vitro” [Mesh] OR “Reproductive Techniques, Assisted” [Mesh] OR “Fertilization in Vitro” OR “In Vitro Fertilization” OR “IVF” OR “In Vitro Fertilizations” OR “Test-Tube Fertilization” OR “Test Tube Fertilization” OR “Test-Tube Fertilizations” [tiab] OR “Fertilizations in Vitro” OR “Test-Tube Babies” OR “Test Tube Babies” OR “Test-Tube Baby” OR “extracorporeal fertilization” OR “in vitro fertilization” OR “testtube baby” [tiab]) AND (“Luteal Phase” [Mesh] OR “Follicular Phase” [Mesh] OR “Luteal Phase” OR “random” OR “immediate” OR “Menstrual Secretory Phase” [tiab] OR “Postovulatory Phase” OR “Follicular Phase” OR “Menstrual Proliferative Phase” OR “Preovulatory Phase”) NOT ((“Animals” [Mesh]) NOT (“Animals” [Mesh] AND “Humans” [Mesh]))

=203 results, 187 after limiting to English on 9/27/2013

Updated results = 39 results, 37 after limiting to English between 9/28/2013–7/13/2015

Embase

“neoplasm”/exp OR neoplasm OR neoplasms OR cancer OR cancers OR neoplasia OR neoplasias OR carcinoma OR carcinomas OR sarcoma OR sarcomas OR tumor OR tumors OR tumour OR tumours AND (“fertilization in vitro”/exp OR “infertility therapy”/exp OR “Fertilization in Vitro” OR “In Vitro Fertilization” OR “IVF” OR “In Vitro Fertilizations” OR “Test-Tube Fertilization” OR “Test Tube Fertilization” OR “Test-Tube Fertilizations” OR “Fertilizations in Vitro” OR “Test-Tube Babies” OR “Test Tube Babies” OR “Test-Tube Baby” OR “extracorporeal fertilization” OR “in vitro fertilization” OR “testtube baby”) AND (“random” OR “immediate” OR “luteal phase”/exp OR “Luteal Phase” OR “Menstrual Secretory Phase” OR “Postovulatory Phase” OR “follicular phase”/exp OR “Follicular Phase” OR “Menstrual Proliferative Phase” OR “Preovulatory Phase”) NOT ([animals]/lim NOT [humans]/lim)

=217 results, 205 after limiting to English on 9/27/2013

Updated results = 63 results (same number after limiting to English) after limiting to 9/28/2013–7/13/2015

Scopus

(TITLE-ABS-KEY (neoplasm OR neoplasms OR cancer* OR neoplasia* OR carcinoma* OR sarcoma* OR “neoplastic disease”)) AND (TITLE-ABS-KEY (“Fertilization in Vitro” OR “In Vitro Fertilization” OR “IVF” OR “In Vitro Fertilizations” OR “Test-Tube Fertilization” OR “Test Tube Fertilization” OR “Test-Tube Fertilizations” OR “Fertilizations in Vitro” OR “Test-Tube Babies” OR “Test Tube Babies” OR “Test-Tube Baby” OR “extracorporeal fertilization” OR “in vitro fertilization” OR “testtube baby”)) AND (“random start” OR “immediate start” OR “Luteal Phase” OR “Menstrual Secretory Phase” OR “Postovulatory Phase” OR “Follicular Phase” OR “Menstrual Proliferative Phase” OR “Preovulatory Phase”) AND (LIMIT-TO(LANGUAGE, “English”))

=156 results, 140 after limiting to English on 10/2/2013

Updated results

*Note: You cannot limit a Scopus search to a day/month/year date. You can only limit by year. I have limited from 2013–present, so there may be some repeat articles from the initial search.

=46 results, 45 after limiting to English on 7/13/2015

Cochrane Library

“Neoplasms” [Mesh] OR “neoplasm” OR “neoplasms” OR “cancer” OR “cancers” OR “neoplasia” OR “neoplasias” OR “carcinoma” OR “sarcoma” OR “sarcomas” OR “neoplastic disease”

AND (“Fertilization in Vitro” [Mesh] OR “Reproductive Techniques, Assisted” [Mesh] OR “Fertilization in Vitro” OR “In Vitro Fertilization” OR “IVF” OR “In Vitro Fertilizations” OR “Test-Tube Fertilization” OR “Test Tube Fertilization” OR “Test-Tube Fertilizations” OR “Fertilizations in Vitro” OR “Test-Tube Babies” OR “Test Tube Babies” OR “Test-Tube Baby” OR “extracorporeal fertilization” OR “in vitro fertilization” OR “testtube baby”)

AND (“random” OR “immediate” OR “Luteal Phase” [Mesh] OR “Luteal Phase” OR “Menstrual Secretory Phase” OR “Postovulatory Phase” OR “Follicular Phase” [Mesh] OR “Follicular Phase” OR “Menstrual Proliferative Phase” OR “Preovulatory Phase”)

Cochrane results = 88 citations (46 Cochrane Reviews, 10 other reviews, 30 trials, 1 economic evaluation, and 1 Cochrane group. Cochrane Group info won’t be included in Endnote library) on 10/2/13

Updated results

Note: There is no way to limit by date in the Cochrane Library. I have included all citations from 10/2013 to the present.

=19 Cochrane reviews and 5 CENTRAL clinical trials on 7/13/2015

ClinicalTrials.gov

(cancer OR neoplasms OR carcinoma OR sarcoma) AND (“IVF” OR “In Vitro Fertilization” OR “Fertilization in Vitro”) AND (“random” OR “immediate” OR “Luteal Phase” OR “Follicular Phase”)

=37 studies on 10/2/13, only 1 of the 37 studies is relevant to your research question (only 1 study addresses cancer and fertility) on 10/2/2013

Updated search: I did not find any new results since the initial search.

ProQuest dissertations and theses

(AB, TI (cancer OR neoplasms OR carcinoma OR sarcoma)) AND (AB, TI (“IVF” OR “In Vitro Fertilization” OR “Fertilization in Vitro”)) AND (AB, TI (“random” OR “immediate” OR “Luteal Phase” OR “Follicular Phase”))

=15 results on 10/2/13

Proceedings

kw: Cancer and (kw: In w Vitro w Fertilization OR kw: IVF) and (kw: random OR kw: immediate OR kw: luteal w phase OR kw: follicular w phase) = 57 results on 10/2/2013

In each of the results I searched for the term “Cancer” within the proceedings to find relevant results. Below you will find the most relevant proceedings abstracts. I can also send you a complete list of results if you would like to review them all. I do not include these in the EndNote library because they don’t format well for the library.

Society for Gynecologic Investigation; Scientific program & abstracts

Conference: Annual meeting; 60th (2013; Mar: Orlando, FL)

Sponsor: Society for Gynecologic Investigation

Publication: Thousand Oaks, Calif.; Sage; [2013]

Language: English

Series: REPRODUCTIVE SCIENCES; 2013; VOL 20; NUMB 3; SUPP;

CN084316501 Author(s): Pavone, M.E.; Hirshfeld-Cytron, J.; Lawson, A.; Smith, K.; Klock, S. Title: Fertility preservation outcomes may differ by cancer diagnosis page(s): p. S-036

ASRM 2010: scientific abstracts to be presented at the Annual Meeting of the American Society for Reproductive Medicine

Conference: Annual meeting (2010; Oct: Denver, CO)

Sponsor: American Society for Reproductive Medicine

Publication: Elsevier Science; 2010

Language: English

Series: FERTILITY AND STERILITY -INTERNATIONAL EDITION-; 2010; VOL 94; NUMB 4; SUPP;

CN080327315 Author(s): Oktay, K.; Lee, S.; Kim, J. Y.; Moy, F. Title: Long-term outcomes and safety of letrozole-FSH protocol in women with breast cancer undergoing fertility preservation: a prospective-controlled study Page(s): p. S11

CN080332413 Author(s): Oktay, K.; Lee, S. Title: Does higher starting dose of FSH stimulation improve fertility preservation cycle outcomes in women with breast cancer? Page(s): p. S160

American Society for Reproductive Medicine

Conference: Annual meeting; 63rd (2007; Oct: Washington, DC)

Sponsor: American Society for Reproductive Medicine

Publication: Elsevier; 2007

Language: English

Series: FERTILITY AND STERILITY -INTERNATIONAL EDITION-; 2007; VOL 88; SUPPL 1;

CN065945755 Author(s): Azim, A. M.; Oktay, K. Title: Safety of ovarian stimulation with letrozole and gonadotropins in breast cancer patients undergoing embryo or oocyte cryopreservation: a prospective controlled study Page(s): p. S33

CN065954823 Author(s): Elizur, S. E.; Holzer, H. E.; Demirtas, E.; Chian, R. C.; Son, W. Y.; Tan, S. L. Title: In vitro maturation (IVM) and vitrification of oocytes retrieved at the luteal phase in cancer patients facing urgent gonadotoxic treatment Page(s): p. S340

Innovative techniques in human embryo viability assessment

Conference: Symposium (2008)

Publication: Cambridge; RBM Online; 2008

Language: English

Series: REPRODUCTIVE BIOMEDICINE ONLINE -PRINT EDITION-; 2008; VOL 17; NUMB 4;

CN069933165 Author(s): Demirtas, E.; Elizur, S.E.; Holzer, H.; Gidoni, Y.; Son, W.-Y.; Chian, R.-C.; Tan, S.L. Title: Case report: Immature oocyte retrieval in the luteal phase to preserve fertility in cancer patients Page(s): p. 520–523

American Society for Reproductive Medicine; ASRM 2003

Conference: Annual meeting; 59th (2003; Oct: San Antonio, TX)

Sponsor: American Society for Reproductive Medicine

Publication: American Society for Reproductive Medicine; 2003

Language: English

Series: FERTILITY AND STERILITY -INTERNATIONAL EDITION-; 2003; VOL 80; SUPPL 3;

CN050026279 Author(s): Meirow, D.; Maman, E.; Farber, B.; Kaufman, B.; Dor, J. Title: fertility preservation using art and embryo cryopreservation prior to chemotherapy in breast cancer patients. new and safe protocol for ovarian stimulation Page(s): p. P-15

Google Scholar

(Cancer) AND (“IVF” OR “in vitro fertilization”) AND (“random start” OR “immediate start” OR “luteal phase” OR “follicular phase”)

=8, 190 results. I reviewed around 20 pages of results (200 citations) before the results were no longer relevant. I found 2 relevant citations that were not already in the EndNote library and added those to the citation list.

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Boots, C.E., Meister, M., Cooper, A.R. et al. Ovarian stimulation in the luteal phase: systematic review and meta-analysis. J Assist Reprod Genet 33, 971–980 (2016). https://doi.org/10.1007/s10815-016-0721-5

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