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The Influence of Cesarean Delivery on Ovarian Reserve: a Prospective Cohort Study

Abstract

To assess the association between cesarean delivery and ovarian reserve, as compared to vaginal delivery. A prospective case control study conducted at a single tertiary medical center between June 2018 and June 2019. Study population included women with singleton pregnancy that underwent first cesarean delivery that were compared to women undergoing normal vaginal delivery. Women with low ovarian reserve, endometriosis, previous pelvic surgery, chronic maternal disease, and active labor were excluded. Ovarian reserve was estimated by Anti-Mullerian hormone (AMH) levels that was determined twice for each participant: up to a week before and 3 months after delivery. Primary outcome was defined as the delta in AMH levels. Data were analyzed by non-parametric tests. During the study period, 135 women were enrolled, of them 63 (47%) underwent cesarean delivery and 72 (53%) had vaginal delivery. Women in the cesarean delivery group were older (34 (31–38) vs. 32 (29–35); p = 0.001); nevertheless, AMH levels measured before delivery were comparable between the two groups (0.92 (0.51–1.79) vs. 0.95 (0.51–1.79) pg/mL; p = 0.42). AMH levels measured after delivery were more than doubled in the study and control groups (2.15 (1.24–3.05) vs. 2.62 (1.05–5.09); p = 0.50), and delta AMH levels were also found comparable (1.25 (0.61–2.22) vs. 1.59 (0.63–3.41), respectively; p = 0.43). Linear regression analysis including age, mode of delivery, gestational age at delivery, and delta hemoglobin levels revealed that only maternal age was significantly associated with delta in AMH levels (B =  − 0.09, p = 0.04). Cesarean delivery does not decrease ovarian reserve as estimated by AMH.

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Data will be available upon request.

References

  1. Taffel SM, Placek PJ, Liss T. Trends in the United States cesarean section rate and reasons for the 1980–85 rise. Am J Public Health. 1987;77(8):955–9.

    Article  CAS  Google Scholar 

  2. Gregory KD, Curtin SC, Taffel SM, Notzon FC. Changes in indications for cesarean delivery: United States, 1985 and 1994. Am J Public Health. 1998;88(9):1384–7.

    Article  CAS  Google Scholar 

  3. Porter M, Bhattacharya S, van Teijlingen E, Templeton A, Group ROFCSRC. Does Caesarean section cause infertility? Hum Reprod. 2003;18(10):1983–6.

    Article  Google Scholar 

  4. Murphy DJ, Stirrat GM, Heron J, Team AS. The relationship between Caesarean section and subfertility in a population-based sample of 14 541 pregnancies. Hum Reprod. 2002;17(7):1914–7.

    Article  CAS  Google Scholar 

  5. Hall MH, Campbell DM, Fraser C, Lemon J. Mode of delivery and future fertility. Br J Obstet Gynaecol. 1989;96(11):1297–303.

    Article  CAS  Google Scholar 

  6. Evers EC, McDermott KC, Blomquist JL, Handa VL. Mode of delivery and subsequent fertility. Hum Reprod. 2014;29(11):2569–74.

    Article  CAS  Google Scholar 

  7. Smith GC, Wood AM, Pell JP, Dobbie R. First cesarean birth and subsequent fertility. Fertil Steril. 2006;85(1):90–5.

    Article  Google Scholar 

  8. Kjerulff KH, Zhu J, Weisman CS, Ananth CV. First birth Caesarean section and subsequent fertility: a population-based study in the USA, 2000–2008. Hum Reprod. 2013;28(12):3349–57.

    Article  CAS  Google Scholar 

  9. Elvander C, Dahlberg J, Andersson G, Cnattingius S. Mode of delivery and the probability of subsequent childbearing: a population-based register study. BJOG. 2015;122(12):1593–600.

    Article  CAS  Google Scholar 

  10. Radin RG, Mikkelsen EM, Rothman KJ, Hatch EE, Sorensen HT, Riis AH, et al. Brief report: Cesarean delivery and subsequent fecundability. Epidemiology. 2016;27(6):889–93.

    Article  Google Scholar 

  11. Chen Y, Pei H, Chang Y, Chen M, Wang H, Xie H, et al. The impact of endometrioma and laparoscopic cystectomy on ovarian reserve and the exploration of related factors assessed by serum anti-Mullerian hormone: a prospective cohort study. J Ovarian Res. 2014;7:108.

    Article  Google Scholar 

  12. Mostaejeran F, Hamoush Z, Rouholamin S. Evaluation of antimullerian hormone levels before and after laparoscopic management of endometriosis. Adv Biomed Res. 2015;4:182.

    PubMed  PubMed Central  Google Scholar 

  13. Uncu G, Kasapoglu I, Ozerkan K, Seyhan A, Oral Yilmaztepe A, Ata B. Prospective assessment of the impact of endometriomas and their removal on ovarian reserve and determinants of the rate of decline in ovarian reserve. Hum Reprod. 2013;28(8):2140–5.

    Article  CAS  Google Scholar 

  14. Chiang HJ, Lin PY, Huang FJ, Kung FT, Lin YJ, Sung PH, et al. The impact of previous ovarian surgery on ovarian reserve in patients with endometriosis. BMC Womens Health. 2015;15:74.

    Article  Google Scholar 

  15. Kröncke T, David M. Uterine artery embolization (UAE) for myoma treatment–results of the 3rd radiologic gynecologic expert meeting. Rofo. 2010;182(7):615–7.

    Article  Google Scholar 

  16. Steiner AZ, Herring AH, Kesner JS, Meadows JW, Stanczyk FZ, Hoberman S, et al. Antimüllerian hormone as a predictor of natural fecundability in women aged 30–42 years. Obstet Gynecol. 2011;117(4):798–804.

    Article  CAS  Google Scholar 

  17. Depmann M, et al. Does AMH relate to timing of menopause? Results of an individual patient data meta- analysis. J Clin Endocrinol Metab. 2018.

  18. Moolhuijsen LME, Visser JA. Anti-Müllerian hormone and ovarian reserve: update on assessing ovarian function. J Clin Endocrinol Metab. 2020;105(11).

  19. Steiner AZ, Pritchard D, Stanczyk FZ, Kesner JS, Meadows JW, Herring AH, et al. Association between biomarkers of ovarian reserve and infertility among older women of reproductive age. JAMA. 2017;318(14):1367–76.

    Article  CAS  Google Scholar 

  20. Haadsma ML, Bukman A, Groen H, Roeloffzen EM, Groenewoud ER, Heineman MJ, et al. The number of small antral follicles (2–6 mm) determines the outcome of endocrine ovarian reserve tests in a subfertile population. Hum Reprod. 2007;22(7):1925–31.

    Article  CAS  Google Scholar 

  21. Zarek SM, Mitchell EM, Sjaarda LA, Mumford SL, Silver RM, Stanford JB, et al. Is Anti-Müllerian Hormone associated with fecundability? Findings from the EAGeR trial. J Clin Endocrinol Metab. 2015;100(11):4215–21.

    Article  CAS  Google Scholar 

  22. Weenen C, Laven JS, Von Bergh AR, Cranfield M, Groome NP, Visser JA, et al. Anti-Müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol Hum Reprod. 2004;10(2):77–83.

    Article  CAS  Google Scholar 

  23. Broekmans FJ, Kwee J, Hendriks DJ, Mol BW, Lambalk CB. A systematic review of tests predicting ovarian reserve and IVF outcome. Hum Reprod Update. 2006;12(6):685–718.

    Article  CAS  Google Scholar 

  24. van Rooij IA, Broekmans FJ, te Velde ER, Fauser BC, Bancsi LF, de Jong FH, et al. Serum anti-Müllerian hormone levels: a novel measure of ovarian reserve. Hum Reprod. 2002;17(12):3065–71.

    Article  Google Scholar 

  25. Baird DD, Dunson DB, Hill MC, Cousins D, Schectman JM. High cumulative incidence of uterine leiomyoma in black and white women: ultrasound evidence. Am J Obstet Gynecol. 2003;188(1):100–7.

    Article  Google Scholar 

  26. Shebl O, Ebner T, Sir A, Schreier-Lechner E, Mayer RB, Tews G, et al. Age-related distribution of basal serum AMH level in women of reproductive age and a presumably healthy cohort. Fertil Steril. 2011;95(2):832–4.

    Article  CAS  Google Scholar 

  27. Ganer Herman H, Gluck O, Keidar R, Kerner R, Kovo M, Levran D, et al. Ovarian reserve following cesarean section with salpingectomy vs tubal ligation: a randomized trial. Am J Obstet Gynecol. 2017;217(4):472.e1-.e6.

    Article  Google Scholar 

  28. Landersoe SK, Larsen EC, Forman JL, Birch Petersen K, Kroman MS, Frederiksen H, et al. Ovarian reserve markers and endocrine profile during oral contraception: is there a link between the degree of ovarian suppression and AMH? Gynecol Endocrinol. 2020;36(12):1090–5.

    Article  CAS  Google Scholar 

  29. Moini A, Pirjani R, Rabiei M, Nurzadeh M, Sepidarkish M, Hosseini R, et al. Can delivery mode influence future ovarian reserve? Anti-Mullerian hormone levels and antral follicle count following cesarean section: a prospective cohort study. J Ovarian Res. 2019;12(1):83.

    Article  Google Scholar 

  30. Gottvall K, Waldenström U. Does a traumatic birth experience have an impact on future reproduction? BJOG. 2002;109(3):254–60.

    Article  Google Scholar 

  31. Eijsink JJ, van der Leeuw-Harmsen L, van der Linden PJ. Pregnancy after Caesarean section: fewer or later? Hum Reprod. 2008;23(3):543–7.

    Article  CAS  Google Scholar 

  32. van Houten EL, Themmen AP, Visser JA. Anti-Müllerian hormone (AMH): regulator and marker of ovarian function. Ann Endocrinol (Paris). 2010;71(3):191–7.

    Article  Google Scholar 

  33. Broer SL, Broekmans FJ, Laven JS, Fauser BC. Anti-Müllerian hormone: ovarian reserve testing and its potential clinical implications. Hum Reprod Update. 2014;20(5):688–701.

    Article  CAS  Google Scholar 

  34. La Marca A, Giulini S, Orvieto R, De Leo V, Volpe A. Anti-Müllerian hormone concentrations in maternal serum during pregnancy. Hum Reprod. 2005;20(6):1569–72.

    Article  Google Scholar 

  35. Grynnerup AG, Lindhard A, Sørensen S. The role of anti-Müllerian hormone in female fertility and infertility - an overview. Acta Obstet Gynecol Scand. 2012;91(11):1252–60.

    Article  Google Scholar 

  36. Stegmann BJ, Santillan M, Leader B, Smith E, Santillan D. Changes in antimüllerian hormone levels in early pregnancy are associated with preterm birth. Fertil Steril. 2015;104(2):347-55.e3.

    Article  CAS  Google Scholar 

  37. Nelson SM, Stewart F, Fleming R, Freeman DJ. Longitudinal assessment of antimüllerian hormone during pregnancy-relationship with maternal adiposity, insulin, and adiponectin. Fertil Steril. 2010;93(4):1356–8.

    Article  CAS  Google Scholar 

  38. Köninger A, Kauth A, Schmidt B, Schmidt M, Yerlikaya G, Kasimir-Bauer S, et al. Anti-Mullerian-hormone levels during pregnancy and postpartum. Reprod Biol Endocrinol. 2013;11:60.

    Article  Google Scholar 

  39. Weghofer A, Dietrich W, Ortner I, Bieglmayer C, Barad D, Gleicher N. Anti-Mullerian hormone levels decline under hormonal suppression: a prospective analysis in fertile women after delivery. Reprod Biol Endocrinol. 2011;9:98.

    Article  CAS  Google Scholar 

  40. Lee TH, Liu CH, Huang CC, Hsieh KC, Lin PM, Lee MS. Impact of female age and male infertility on ovarian reserve markers to predict outcome of assisted reproduction technology cycles. Reprod Biol Endocrinol. 2009;7:100.

    Article  Google Scholar 

  41. Lambalk CB, van Disseldorp J, de Koning CH, Broekmans FJ. Testing ovarian reserve to predict age at menopause. Maturitas. 2009;63(4):280–91.

    Article  CAS  Google Scholar 

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Acknowledgements

We acknowledge the Endocrine Laboratory Team of Sheba Medical Center for their cooperation.

Author information

Authors and Affiliations

Authors

Contributions

Aya Mohr-Sasson- conceptualization; formal analysis; investigation; methodology; project administration; writing – original draft.

Jigal Haas- methodology, investigation, review and editing.

Sonya Bar-Adon- investigation.

Maya Shats- investigation.

Roni Hochman- data collecting, investigation.

Raoul Orvieto- methodology; review and editing.

Shali Mazaki-Tovi- methodology, writing—editing.

Eyal Sivan- methodology; project administration; supervision; writing—review and editing.

Corresponding author

Correspondence to Aya Mohr-Sasson.

Ethics declarations

Ethics Approval

The study protocol was approved by the Institutional Review Board (ID 5125–18 SMC) on the 30th of May 2018 and was registered at the National Institutes of Health (NCT02821702). All women signed written informed consent to participate in the study.

Consent to Participate

All participants signed informed consent before participating in the study.

Consent for Publication

All authors gave consent for publication.

Conflict of Interest

The authors declare no competing interests.

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Cite this article

Mohr-Sasson, A., Haas, J., Bar-Adon, S. et al. The Influence of Cesarean Delivery on Ovarian Reserve: a Prospective Cohort Study. Reprod. Sci. 29, 639–645 (2022). https://doi.org/10.1007/s43032-021-00730-z

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  • DOI: https://doi.org/10.1007/s43032-021-00730-z

Keywords

  • Cesarean delivery
  • Fertility
  • Anti-Mullerian hormone
  • Ovarian reserve
  • Vaginal delivery