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Pregnancy and Live Birth Rates Are Comparable in Young Infertile Women Presenting with Severe Endometriosis and Tubal Infertility

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Abstract

The aim of this study is to evaluate the effect of severe endometriosis in younger patients compared to tubal infertility on pregnancy and live birth rate undergoing in vitro fertilization (IVF). This prospective observational study included 294 women with severe endometriosis and 358 women with tubal factor as control who underwent IVF. Follicular fluid samples were collected during oocyte retrieval, and cytokines and angiogenic factors were estimated. The groups were sub-stratified based on age. Number of metaphase II oocytes, grade I/II embryos, pregnancy rate, miscarriage rate per pregnancy, and live birth rate were compared. Significantly elevated levels of cytokines and angiogenic molecules were observed in younger endometriosis patients when compared to tubal group (p < 0.001). Number of MII oocytes (p < 0.003) and grade I/II embryos (p < 0.001) were observed to be significantly lower in these women when compared with matched controls. Despite higher levels of inflammatory cytokines, angiogenic molecules, fewer MII oocytes, and grade I/II embryos, the younger endometriosis patients had similar pregnancy (OR 0.81; 95% CI 0.54–1.22; p = 0.31) and live birth rate (OR 0.78; 95% CI 0.5–1.2; p = 0.26) when compared with matched controls. In contrast, endometriosis patients of age ≥ 35 years had significantly less likelihood of live birth (OR 0.47; 95% CI 0.25–0.9; p = 0.02) and pregnancy rate (OR 0.46; 95% CI 0.22–0.95; p = 0.03), respectively, when compared with the matched controls. It appears that women with severe endometriosis have even chance of successful pregnancy if diagnosed at early age and sought for assisted reproductive technology to reduce its adverse effect on reproductive outcome.

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References

  1. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin N Am. 1997;24(2):235–58.

    Article  CAS  Google Scholar 

  2. Meuleman C, Vandenabeele B, Fieuws S, Spiessens C, Timmerman D, D'Hooghe T. High prevalence of endometriosis in infertile women with normal ovulation and normospermic partners. Fertil Steril. 2009;92(1):68–74.

    Article  PubMed  Google Scholar 

  3. Adamson GD. Endometriosis fertility index: is it better than the present staging systems? Curr Opin Obstet Gynecol. 2013;25(3):186–92.

    Article  PubMed  Google Scholar 

  4. Vercellini P, Consonni D, Dridi D, Bracco B, Frattaruolo MP, Somigliana E. Uterine adenomyosis and in vitro fertilization outcome: a systematic review and meta-analysis. Hum Reprod. 2014;29(5):964–77.

    Article  PubMed  Google Scholar 

  5. Young VJ, Brown JK, Saunders PT, Horne AW. The role of the peritoneum in the pathogenesis of endometriosis. Hum Reprod Update. 2013;19(5):558–69.

    Article  PubMed  Google Scholar 

  6. Laux-Biehlmann A, d'Hooghe T, Zollner TM. Menstruation pulls the trigger for inflammation and pain in endometriosis. Trends Pharmacol Sci. 2015;36(5):270–6.

    Article  CAS  PubMed  Google Scholar 

  7. Berbic M, Fraser IS. Regulatory T cells and other leukocytes in the pathogenesis of endometriosis. J Reprod Immunol. 2011;88(2):149–55.

    Article  CAS  PubMed  Google Scholar 

  8. Fazleabas AT, Braundmeier A, Parkin K. Endometriosis-induced changes in regulatory T cells - insights towards developing permanent contraception. Contraception. 2015;92(2):116–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Gazvani R, Templeton A. Peritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis. Reproduction. 2002;123(2):217–26.

    Article  CAS  PubMed  Google Scholar 

  10. Iwabe T, Harada T, Terakawa N. Role of cytokines in endometriosis-associated infertility. Gynecol Obstet Investig. 2002;53(Suppl 1):19–25.

    Article  CAS  Google Scholar 

  11. Matsuzaki S, Schubert B. Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis. Fertil Steril. 2010;93(7):2431–2.

    Article  PubMed  Google Scholar 

  12. Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S. The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol. 2012;10:49.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Gupta S, Agarwal A, Agarwal R, Loret de Mola JR. Impact of ovarian endometrioma on assisted reproduction outcomes. Reprod BioMed Online. 2006;13(3):349–60.

    Article  PubMed  Google Scholar 

  14. Pellicer A, Albert C, Garrido N, Navarro J, Remohi J, Simon C. The pathophysiology of endometriosis-associated infertility: follicular environment and embryo quality. J Reprod Fertil Suppl. 2000;55:109–19.

    CAS  PubMed  Google Scholar 

  15. Velasco I, Acien P, Campos A, Acien MI, Ruiz-Macia E. Interleukin-6 and other soluble factors in peritoneal fluid and endometriomas and their relation to pain and aromatase expression. J Reprod Immunol. 2010;84(2):199–205.

    Article  CAS  PubMed  Google Scholar 

  16. Lebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil Steril. 2001;75(1):1–10.

    Article  CAS  PubMed  Google Scholar 

  17. Kitajima M, Dolmans MM, Donnez O, Masuzaki H, Soares M, Donnez J. Enhanced follicular recruitment and atresia in cortex derived from ovaries with endometriomas. Fertil Steril. 2014;101(4):1031–7.

    Article  PubMed  Google Scholar 

  18. Lin XN, Wei ML, Tong XM, Xu WH, Zhou F, Huang QX, et al. Outcome of in vitro fertilization in endometriosis-associated infertility: a 5-year database cohort study. Chin Med J. 2012;125(15):2688–93.

    CAS  PubMed  Google Scholar 

  19. Suzuki T, Izumi S, Matsubayashi H, Awaji H, Yoshikata K, Makino T. Impact of ovarian endometrioma on oocytes and pregnancy outcome in in vitro fertilization. Fertil Steril. 2005;83(4):908–13.

    Article  PubMed  Google Scholar 

  20. Muteshi CM, Ohuma EO, Child T, Becker CM. The effect of endometriosis on live birth rate and other reproductive outcomes in ART cycles: a cohort study. Human Reprod Open. 2018;2018(4):hoy016.

    Article  Google Scholar 

  21. Opoien HK, Fedorcsak P, Omland AK, et al. In vitro fertilization is a successful treatment in endometriosis-associated infertility. Fertil Steril. 2012;97(4):912–8.

    Article  PubMed  Google Scholar 

  22. Reinblatt SL, Ishai L, Shehata F, Son WY, Tulandi T, Almog B. Effects of ovarian endometrioma on embryo quality. Fertil Steril. 2011;95(8):2700–2.

    Article  PubMed  Google Scholar 

  23. Garcia-Velasco JA, Arici A. Is the endometrium or oocyte/embryo affected in endometriosis? Hum Reprod. 1999;14(Suppl 2):77–89.

    Article  PubMed  Google Scholar 

  24. ASRM. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril. 1997;67(5):817–21.

    Article  Google Scholar 

  25. Opoien HK, Fedorcsak P, Polec A, Stensen MH, Abyholm T, Tanbo T. Do endometriomas induce an inflammatory reaction in nearby follicles? Hum Reprod. 2013;28(7):1837–45.

    Article  CAS  PubMed  Google Scholar 

  26. Garcia-Velasco JA, Somigliana E. Management of endometriomas in women requiring IVF: to touch or not to touch. Hum Reprod. 2009;24(3):496–501.

    Article  PubMed  Google Scholar 

  27. Guo H, Wang Y, Chen Q, Chai W, Sun L, Ai A, et al. Use of medroxyprogesterone acetate in women with ovarian endometriosis undergoing controlled ovarian hyperstimulation for in vitro fertilization. Sci Rep. 2017;7(1):11927.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Giudice LC, Kao LC. Endometriosis. Lancet. 2004;364(9447):1789–99.

    Article  PubMed  Google Scholar 

  29. Farquhar C. Endometriosis. BMJ. 2007;334(7587):249–53.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Holoch KJ, Lessey BA. Endometriosis and infertility. Clin Obstet Gynecol. 2010;53(2):429–38.

    Article  PubMed  Google Scholar 

  31. Sanchez AM, Vigano P, Somigliana E, Panina-Bordignon P, Vercellini P, Candiani M. The distinguishing cellular and molecular features of the endometriotic ovarian cyst: from pathophysiology to the potential endometrioma-mediated damage to the ovary. Hum Reprod Update. 2014;20(2):217–30.

    Article  CAS  PubMed  Google Scholar 

  32. Bryan N, Ahswin H, Smart N, Bayon Y, Wohlert S, Hunt JA. Reactive oxygen species (ROS)--a family of fate deciding molecules pivotal in constructive inflammation and wound healing. Eur Cell Mater. 2012;24:249–65.

    Article  CAS  PubMed  Google Scholar 

  33. Lo Turco EG, Souza GH, Garcia JS, Ferreira CR, Eberlin MN, Bertolla RP. Effect of endometriosis on the protein expression pattern of follicular fluid from patients submitted to controlled ovarian hyperstimulation for in vitro fertilization. Hum Reprod. 2010;25(7):1755–66.

    Article  PubMed  CAS  Google Scholar 

  34. Singh AK, Dutta M, Chattopadhyay R, Chakravarty B, Chaudhury K. Intrafollicular interleukin-8, interleukin-12, and adrenomedullin are the promising prognostic markers of oocyte and embryo quality in women with endometriosis. J Assist Reprod Genet. 2016;33(10):1363–72.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Malutan AM, Drugan T, Costin N, Ciortea R, Bucuri C, Rada MP, et al. Pro-inflammatory cytokines for evaluation of inflammatory status in endometriosis. Cent Eur J Immunol. 2015;40(1):96–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bulun SE. Endometriosis. N Engl J Med. 2009;360(3):268–79.

    Article  CAS  PubMed  Google Scholar 

  37. Gao MZ, Zhao XM, Lin Y, Sun ZG, Zhang HQ. Effects of EG-VEGF, VEGF and TGF-beta1 on pregnancy outcome in patients undergoing IVF-ET treatment. J Assist Reprod Genet. 2012;29(10):1091–6.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Marinoni E, Feliciani E, Muzzonigro F, Letizia C, Tranquilli A, Tranquilli D, et al. Intrafollicular concentration of adrenomedullin is associated with IVF outcome. Gynecol Endocrinol. 2010;26(6):435–9.

    Article  CAS  PubMed  Google Scholar 

  39. Lambert S, Santulli P, Chouzenoux S, et al. Endometriosis: increasing concentrations of serum interleukin-1beta and interleukin-1sRII is associated with the deep form of this pathology. J Gynecol Obstet Biol Reprod (Paris). 2014;43(9):735–43.

    Article  CAS  Google Scholar 

  40. Santulli P, Borghese B, Chouzenoux S, Vaiman D, Borderie D, Streuli I, et al. Serum and peritoneal interleukin-33 levels are elevated in deeply infiltrating endometriosis. Hum Reprod. 2012;27(7):2001–9.

    Article  CAS  PubMed  Google Scholar 

  41. Yang Y, Zhang X, Zhou C, Huang X, Lin J, Xu H. Elevated immunoreactivity of RANTES and CCR1 correlate with the severity of stages and dysmenorrhea in women with deep infiltrating endometriosis. Acta Histochem. 2013;115(5):434–9.

    Article  CAS  PubMed  Google Scholar 

  42. Wunder DM, Mueller MD, Birkhauser MH, Bersinger NA. Increased ENA-78 in the follicular fluid of patients with endometriosis. Acta Obstet Gynecol Scand. 2006;85(3):336–42.

    Article  CAS  PubMed  Google Scholar 

  43. Hornung D, Ryan IP, Chao VA, Vigne JL, Schriock ED, Taylor RN. Immunolocalization and regulation of the chemokine RANTES in human endometrial and endometriosis tissues and cells. J Clin Endocrinol Metab. 1997;82(5):1621–8.

    CAS  PubMed  Google Scholar 

  44. Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil Steril. 2002;77(6):1148–55.

    Article  PubMed  Google Scholar 

  45. Senapati S, Sammel MD, Morse C, Barnhart KT. Impact of endometriosis on in vitro fertilization outcomes: an evaluation of the Society for Assisted Reproductive Technologies Database. Fertil Steril. 2016;106(1):164–71 e161.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Stern JE, Brown MB, Wantman E, Kalra SK, Luke B. Live birth rates and birth outcomes by diagnosis using linked cycles from the SART CORS database. J Assist Reprod Genet. 2013;30(11):1445–50.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Polat M, Boynukalin FK, Yarali I, Esinler I, Yarali H. Endometriosis is not associated with inferior pregnancy rates in in vitro fertilization: an analysis of 616 patients. Gynecol Obstet Investig. 2014;78(1):59–64.

    Article  Google Scholar 

  48. Roux P, Perrin J, Mancini J, Agostini A, Boubli L, Courbiere B. Factors associated with a poor prognosis for the IVF-ICSI live birth rate in women with rAFS stage III and IV endometriosis. J Assist Reprod Genet. 2017;34(7):921–8.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Gonzalez-Comadran M, Schwarze JE, Zegers-Hochschild F, Souza MD, Carreras R, Checa MA. The impact of endometriosis on the outcome of assisted reproductive technology. Reprod Biol Endocrinol. 2017;15(1):8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Hamdan M, Dunselman G, Li TC, Cheong Y. The impact of endometrioma on IVF/ICSI outcomes: a systematic review and meta-analysis. Hum Reprod Update. 2015;21(6):809–25.

    Article  CAS  PubMed  Google Scholar 

  51. Berlanda N, Alberico D, Barbara G, Frattaruolo MP, Vercellini P. Exploring the relationship between endometriomas and infertility. Women Health. 2015;11(2):127–35.

    Article  CAS  Google Scholar 

  52. Vassilopoulou L, Matalliotakis M, Zervou MI, Matalliotaki C, Spandidos DA, Matalliotakis I, et al. Endometriosis and in vitro fertilisation. Exp Ther Med. 2018;16(2):1043–51.

    PubMed  PubMed Central  Google Scholar 

  53. Muzii L, Di Tucci C, Di Feliciantonio M, Marchetti C, Perniola G, Panici PB. The effect of surgery for endometrioma on ovarian reserve evaluated by antral follicle count: a systematic review and meta-analysis. Hum Reprod. 2014;29(10):2190–8.

    Article  CAS  PubMed  Google Scholar 

  54. Raffi F, Metwally M, Amer S. The impact of excision of ovarian endometrioma on ovarian reserve: a systematic review and meta-analysis. J Clin Endocrinol Metab. 2012;97(9):3146–54.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to acknowledge Dr. Himadri S. Sarkar, Ms. Gunja Bose, and Ms. Sarmistha Kundu Nag of IRM Kolkata for sample and patient data collection. We also like to acknowledge all the patients who voluntarily participated in the study.

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Authors and Affiliations

  1. Institute of Reproductive Medicine, HB-36/A/3, Sector – III, Salt Lake City, Kolkata, 700106, India

    Sunita Sharma, Sourav RoyChoudhury, Shikha Bathwal, Ratnaboli Bhattacharya, Shovandeb Kalapahar, Ratna Chattopadhyay, Indranil Saha & Baidyanath Chakravarty

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  1. Sunita Sharma
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  2. Sourav RoyChoudhury
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  3. Shikha Bathwal
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  4. Ratnaboli Bhattacharya
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  5. Shovandeb Kalapahar
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  6. Ratna Chattopadhyay
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  7. Indranil Saha
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  8. Baidyanath Chakravarty
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Contributions

S Sharma conceived the study and contributed toward the study design, patient selection. S Sharma and S Bathwala performed the study, manuscript drafting, and critical discussion. S RoyChoudhury performed data analysis, manuscript drafting, and critical discussion. R Bhattacharyaa, Shovandeb Kalapahar, and I Saha helped with the data analysis and manuscript drafting. R Chattopadhyaya and BN Chakravartya did critical discussion and proofreading the article.

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Correspondence to Sunita Sharma.

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Sharma, S., RoyChoudhury, S., Bathwal, S. et al. Pregnancy and Live Birth Rates Are Comparable in Young Infertile Women Presenting with Severe Endometriosis and Tubal Infertility. Reprod. Sci. 27, 1340–1349 (2020). https://doi.org/10.1007/s43032-020-00158-x

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  • DOI: https://doi.org/10.1007/s43032-020-00158-x

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