Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2017

Open Access 01-12-2017 | Research

The impact of endometriosis on the outcome of Assisted Reproductive Technology

Authors: Mireia González-Comadran, Juan Enrique Schwarze, Fernando Zegers-Hochschild, Maria do Carmo B. Souza, Ramon Carreras, Miguel Ángel Checa

Published in: Reproductive Biology and Endocrinology | Issue 1/2017

Login to get access

Abstract

Background

Endometriosis has been described to impair fertility through various mechanisms. However, studies evaluating the reproductive outcomes of women undergoing assisted reproductive technologies show controversial results. The aim of this study is to assess whether the reproductive outcome is impaired among women with endometriosis-associated infertility undergoing IVF.

Methods

A retrospective cohort study was performed, including women undergoing IVF reported by the Red Latinoamericana de Reproduccion Asistida (Redlara) registry, between January 2010 and December 2012. The study group included women with endometriosis-associated infertility, and the control group women with tubal factor, endocrine disorders or unexplained infertility. Women above 40 years, severe male factor and premature ovarian failure were excluded. The reproductive outcomes of between both groups were compared. The primary outcome was live birth. Secondary outcomes included clinical pregnancy, miscarriage, number of oocytes retrieved and number of fertilized oocytes. Outcomes were assessed after the first fresh IVF cycle, and were adjusted for age and number of embryos transferred.

Results

A total of 22.416 women were included (3.583 with endometriosis and 18.833 in the control group). Mean age of patients in the endometriosis group and control group was 34.86 (3.47) and 34.61 (3.91) respectively, p = 0.000. The mean number of oocytes retrieved were 8.89 (6.23) and 9.86 (7.02) respectively, p = 0.000. No significant differences were observed between groups in terms of live birth (odds ratio (OR) 1.032, p = 0.556), clinical pregnancy (OR 1.044, p = 0.428) and miscarriage rates (OR 1.049, p = 0.623). Women with endometriosis had significantly lower number of oocytes retrieved (incidence risk ratio (IRR) 0.917, 95% CI 0.895–0.940), however, the number of fertilized oocytes did not differ among the two groups when adjusting for the number of oocytes retrieved (IRR 1.003, p = 0.794). An age-stratified analysis was performed, and no differences were observed in the reproductive outcomes between groups for women aged under 35 and 35 to 40.

Conclusions

Reproductive outcomes among women undergoing IVF and diagnosed with endometriosis-associated infertility do not differ significantly from women without the disease. Although women with endometriosis generate fewer oocytes, fertilization rate is not impaired and the likelihood of achieving a live birth is also not affected.
Literature
1.
go back to reference Ozkan S, Murk W, Arici A. Endometriosis and infertility: epidemiology and evidence-based treatments. Ann N Y Acad Sci. 2008;1127:92–100.CrossRefPubMed Ozkan S, Murk W, Arici A. Endometriosis and infertility: epidemiology and evidence-based treatments. Ann N Y Acad Sci. 2008;1127:92–100.CrossRefPubMed
2.
go back to reference Hummelshoj L, Prentice A, Groothuis P. Update on endometriosis. Womens Health (Lond Engl). 2006;2(1):53–6.CrossRef Hummelshoj L, Prentice A, Groothuis P. Update on endometriosis. Womens Health (Lond Engl). 2006;2(1):53–6.CrossRef
5.
go back to reference Somigliana E, Viganò P, Tirelli AS, Felicetta I, Torresani E, Vignali M, et al. Use of the concomitant serum dosage of CA 125, CA 19-9 and interleukin-6 to detect the presence of endometriosis. Results from a series of reproductive age women undergoing laparoscopic surgery for benign gynaecological conditions. Hum Reprod. 2004;19(8):1871–6.CrossRefPubMed Somigliana E, Viganò P, Tirelli AS, Felicetta I, Torresani E, Vignali M, et al. Use of the concomitant serum dosage of CA 125, CA 19-9 and interleukin-6 to detect the presence of endometriosis. Results from a series of reproductive age women undergoing laparoscopic surgery for benign gynaecological conditions. Hum Reprod. 2004;19(8):1871–6.CrossRefPubMed
6.
go back to reference Saito H, Seino T, Kaneko T, Nakahara K, Toya M, Kurachi H. Endometriosis and oocyte quality. Gynecol Obstet Invest. 2002;53 Suppl 1:46–51. Review.CrossRefPubMed Saito H, Seino T, Kaneko T, Nakahara K, Toya M, Kurachi H. Endometriosis and oocyte quality. Gynecol Obstet Invest. 2002;53 Suppl 1:46–51. Review.CrossRefPubMed
7.
go back to reference Toya M, Saito H, Ohta N, Saito T, Kaneko T, Hiroi M. Moderate and severe endometriosis is associated with alterations in the cell cycle of granulosa cells in patients undergoing in vitro fertilization and embryo transfer. Fertil Steril. 2000;73(2):344–50.CrossRefPubMed Toya M, Saito H, Ohta N, Saito T, Kaneko T, Hiroi M. Moderate and severe endometriosis is associated with alterations in the cell cycle of granulosa cells in patients undergoing in vitro fertilization and embryo transfer. Fertil Steril. 2000;73(2):344–50.CrossRefPubMed
8.
go back to reference Kissler S, Hamscho N, Zangos S, Gätje R, Müller A, et al. Diminished pregnancy rates in endometriosis due to impaired uterotubal transport assessed by hysterosalpingoscintigraphy. BJOG. 2005;112(10):1391–6.CrossRefPubMed Kissler S, Hamscho N, Zangos S, Gätje R, Müller A, et al. Diminished pregnancy rates in endometriosis due to impaired uterotubal transport assessed by hysterosalpingoscintigraphy. BJOG. 2005;112(10):1391–6.CrossRefPubMed
9.
go back to reference Klemmt PA, Carver JG, Kennedy SH, Koninckx PR, Mardon HJ. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril. 2006;85(3):564–72.CrossRefPubMedPubMedCentral Klemmt PA, Carver JG, Kennedy SH, Koninckx PR, Mardon HJ. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril. 2006;85(3):564–72.CrossRefPubMedPubMedCentral
10.
go back to reference Matsuzaki S, Schubert B. Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis. Fertil Steril. 2010;93(7):2431–2.CrossRefPubMed Matsuzaki S, Schubert B. Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis. Fertil Steril. 2010;93(7):2431–2.CrossRefPubMed
11.
go back to reference Richter ON, Dorn C, Rösing B, Flaskamp C, Ulrich U. Tumor necrosis factor alpha secretion by peritoneal macrophages in patients with endometriosis. Arch Gynecol Obstet. 2005;271(2):143–7.CrossRefPubMed Richter ON, Dorn C, Rösing B, Flaskamp C, Ulrich U. Tumor necrosis factor alpha secretion by peritoneal macrophages in patients with endometriosis. Arch Gynecol Obstet. 2005;271(2):143–7.CrossRefPubMed
12.
go back to reference Garrido N, Navarro J, Remohi J, Simon C, Pellicer A. Follicular hormonal environment and embryo quality in women with endometriosis. Hum Reprod Update. 2000;6:67–74.CrossRefPubMed Garrido N, Navarro J, Remohi J, Simon C, Pellicer A. Follicular hormonal environment and embryo quality in women with endometriosis. Hum Reprod Update. 2000;6:67–74.CrossRefPubMed
13.
go back to reference LinXN WML, Tong XM, Xu WH, Zhou F, Huang QX, et al. Outcome of in vitro fertilization in endometriosis-associated infertility: a 5-year data base cohort study. Chin Med J (Engl). 2012;125(15):2688–93. LinXN WML, Tong XM, Xu WH, Zhou F, Huang QX, et al. Outcome of in vitro fertilization in endometriosis-associated infertility: a 5-year data base cohort study. Chin Med J (Engl). 2012;125(15):2688–93.
14.
go back to reference Kuivasaari P, Hippeläinen M, Anttila M, Heinonen S. Effect of endometriosis on IVF/ICSI outcome: stage III/IV endometriosis worsens cumulative pregnancy and live-born rates. Hum Reprod. 2005;20(11):3130–5.CrossRefPubMed Kuivasaari P, Hippeläinen M, Anttila M, Heinonen S. Effect of endometriosis on IVF/ICSI outcome: stage III/IV endometriosis worsens cumulative pregnancy and live-born rates. Hum Reprod. 2005;20(11):3130–5.CrossRefPubMed
15.
go back to reference Pellicer A, Oliveira N, Ruiz A, Remohí J, Simón C. Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod. 1995;10 Suppl 2:91–7. Review.CrossRefPubMed Pellicer A, Oliveira N, Ruiz A, Remohí J, Simón C. Exploring the mechanism(s) of endometriosis-related infertility: an analysis of embryo development and implantation in assisted reproduction. Hum Reprod. 1995;10 Suppl 2:91–7. Review.CrossRefPubMed
16.
go back to reference Bongioanni F, Revelli A, Gennarelli G, Guidetti D, Delle Piane LD, Holte J. Ovarian endometriomas and IVF: a retrospective case-control study. Reprod Biol Endocrinol. 2011;9:81.CrossRefPubMedPubMedCentral Bongioanni F, Revelli A, Gennarelli G, Guidetti D, Delle Piane LD, Holte J. Ovarian endometriomas and IVF: a retrospective case-control study. Reprod Biol Endocrinol. 2011;9:81.CrossRefPubMedPubMedCentral
17.
go back to reference Ashrafi M, Fakheri T, Kiani K, Sadeghi M, Akhoond MR. Impact of the endometrioma on ovarian response and pregnancy rate in in vitro fertilization cycles. Int J Fertil Steril. 2014;8(1):29–34.PubMedPubMedCentral Ashrafi M, Fakheri T, Kiani K, Sadeghi M, Akhoond MR. Impact of the endometrioma on ovarian response and pregnancy rate in in vitro fertilization cycles. Int J Fertil Steril. 2014;8(1):29–34.PubMedPubMedCentral
18.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
19.
go back to reference Opøien HK, Fedorcsak P, Omland AK, Abyholm T, Bjercke S, Ertzeid G, et al. In vitro fertilization is a successful treatment in endometriosis-associated infertility. Fertil Steril. 2012;97(4):912–8.CrossRefPubMed Opøien HK, Fedorcsak P, Omland AK, Abyholm T, Bjercke S, Ertzeid G, et al. In vitro fertilization is a successful treatment in endometriosis-associated infertility. Fertil Steril. 2012;97(4):912–8.CrossRefPubMed
20.
go back to reference Mathieu d’Argent E, Coutant C, Ballester M, Dessolle L, Bazot M, Antoine JM, et al. Results of first in vitro fertilization cycle in women with colorectal endometriosis compared with those with tubal or male factor infertility. Fertil Steril. 2010;94(6):2441–3.CrossRefPubMed Mathieu d’Argent E, Coutant C, Ballester M, Dessolle L, Bazot M, Antoine JM, et al. Results of first in vitro fertilization cycle in women with colorectal endometriosis compared with those with tubal or male factor infertility. Fertil Steril. 2010;94(6):2441–3.CrossRefPubMed
21.
go back to reference Von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC. Vandenbroucke JP; for the STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: Guidelines for reporting observational studies. Int J Surg. 2014;12(12):1495–9.CrossRef Von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC. Vandenbroucke JP; for the STROBE Initiative. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: Guidelines for reporting observational studies. Int J Surg. 2014;12(12):1495–9.CrossRef
22.
go back to reference Zegers-Hochschild F, Adamson GD, de Mouzon J, Ishihara O, Mansour R. Nygren K, et al; International Committee for Monitoring Assisted Reproductive Technology (ICMART) and The World Health Organization (WHO) revised glossary of ART terminology, 2009. Fertil Steril. 2009;92(5):1520–4.CrossRefPubMed Zegers-Hochschild F, Adamson GD, de Mouzon J, Ishihara O, Mansour R. Nygren K, et al; International Committee for Monitoring Assisted Reproductive Technology (ICMART) and The World Health Organization (WHO) revised glossary of ART terminology, 2009. Fertil Steril. 2009;92(5):1520–4.CrossRefPubMed
23.
go back to reference Farquharson RG, Jauniaux E, Exalto, ESHRE Special Interest Group for Early Pregnancy (SIGEP). Updated and revised nomenclature for description of early pregnancy events. Hum Reprod. 2005;20(11):3008–11.CrossRefPubMed Farquharson RG, Jauniaux E, Exalto, ESHRE Special Interest Group for Early Pregnancy (SIGEP). Updated and revised nomenclature for description of early pregnancy events. Hum Reprod. 2005;20(11):3008–11.CrossRefPubMed
24.
go back to reference Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil Steril. 2002;77(6):1148–55.CrossRefPubMed Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil Steril. 2002;77(6):1148–55.CrossRefPubMed
25.
go back to reference Harb HM, Gallos ID, Chu J, Harb M, Coomarasamy A. The effect of endometriosis on in vitro fertilization outcome: a systematic review and meta-analysis. BJOG. 2013;120(11):1308–20.CrossRefPubMed Harb HM, Gallos ID, Chu J, Harb M, Coomarasamy A. The effect of endometriosis on in vitro fertilization outcome: a systematic review and meta-analysis. BJOG. 2013;120(11):1308–20.CrossRefPubMed
26.
go back to reference Barbosa MA, Teixeira DM, Navarro PA, Ferriani RA, Nastri CO, Martins WP. The impact of endometriosis and its staging on assisted reproduction outcomes: a systematic review and meta-analysis. Ultrasound Obstet Gynecol. 2014;44(3):261–78. 24639087.CrossRefPubMed Barbosa MA, Teixeira DM, Navarro PA, Ferriani RA, Nastri CO, Martins WP. The impact of endometriosis and its staging on assisted reproduction outcomes: a systematic review and meta-analysis. Ultrasound Obstet Gynecol. 2014;44(3):261–78. 24639087.CrossRefPubMed
27.
go back to reference Ballester M, Oppenheimer A, Mathieu d’Argent E, Touboul C, Antoine JM, Nisolle M, et al. Deep infiltrating endometriosis is a determinant factor of cumulative pregnancy rate after intracytoplasmic sperm injection/in vitro fertilization cycles in patients with endometriomas. Fertil Steril. 2012;97(2):367–72.CrossRefPubMed Ballester M, Oppenheimer A, Mathieu d’Argent E, Touboul C, Antoine JM, Nisolle M, et al. Deep infiltrating endometriosis is a determinant factor of cumulative pregnancy rate after intracytoplasmic sperm injection/in vitro fertilization cycles in patients with endometriomas. Fertil Steril. 2012;97(2):367–72.CrossRefPubMed
28.
go back to reference Somigliana E, Infantino M, Benedetti F, Arnoldi M, Calanna G, Ragni G. The presence of ovarian endometriomas is associated with a reduced responsiveness to gonadotropins. Fertil Steril. 2006;86(1):192–6.CrossRefPubMed Somigliana E, Infantino M, Benedetti F, Arnoldi M, Calanna G, Ragni G. The presence of ovarian endometriomas is associated with a reduced responsiveness to gonadotropins. Fertil Steril. 2006;86(1):192–6.CrossRefPubMed
29.
go back to reference Burney RO, Talbi S, Hamilton AE, Vo KC, Nyegaard M, et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology. 2007;148(8):3814–26.CrossRefPubMed Burney RO, Talbi S, Hamilton AE, Vo KC, Nyegaard M, et al. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology. 2007;148(8):3814–26.CrossRefPubMed
30.
go back to reference Dimitriadis E, Stoikos C, Stafford-Bell M, Clark I, Paiva P, et al. Interleukin-11, IL-1 receptor alpha and leukemia inhibitory factor are dysregulated in endometrium of infertile women with endometriosis during the implantation window. J Reprod Immunol. 2006;69(1):56–64.CrossRef Dimitriadis E, Stoikos C, Stafford-Bell M, Clark I, Paiva P, et al. Interleukin-11, IL-1 receptor alpha and leukemia inhibitory factor are dysregulated in endometrium of infertile women with endometriosis during the implantation window. J Reprod Immunol. 2006;69(1):56–64.CrossRef
31.
go back to reference Lee B, Du H, Taylor HS. Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod. 2009;80(1):79–85.CrossRefPubMedPubMedCentral Lee B, Du H, Taylor HS. Experimental murine endometriosis induces DNA methylation and altered gene expression in eutopic endometrium. Biol Reprod. 2009;80(1):79–85.CrossRefPubMedPubMedCentral
32.
go back to reference Díaz I, Navarro J, Blasco L, Simón C, Pellicer A, Remohí J. Impact of stageIII-IV endometriosis on recipients of sibling oocytes: matched case-control study. Fertil Steril. 2000;74(1):31–4.CrossRefPubMed Díaz I, Navarro J, Blasco L, Simón C, Pellicer A, Remohí J. Impact of stageIII-IV endometriosis on recipients of sibling oocytes: matched case-control study. Fertil Steril. 2000;74(1):31–4.CrossRefPubMed
33.
go back to reference Simón C, Gutiérrez A, Vidal A, de los Santos MJ, Tarín JJ, Remohí J, et al. Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod. 1994;9(4):725–9.PubMed Simón C, Gutiérrez A, Vidal A, de los Santos MJ, Tarín JJ, Remohí J, et al. Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod. 1994;9(4):725–9.PubMed
34.
go back to reference Katsoff B, Check JH, Davies E, Wilson C. Evaluation of the effect of endometriosis on oocyte quality and endometrial environment by comparison of donor and recipient outcomes following embryo transfer in a shared oocyte program. Clin Exp Obstet Gynecol. 2006;33(4):201–2.PubMed Katsoff B, Check JH, Davies E, Wilson C. Evaluation of the effect of endometriosis on oocyte quality and endometrial environment by comparison of donor and recipient outcomes following embryo transfer in a shared oocyte program. Clin Exp Obstet Gynecol. 2006;33(4):201–2.PubMed
Metadata
Title
The impact of endometriosis on the outcome of Assisted Reproductive Technology
Authors
Mireia González-Comadran
Juan Enrique Schwarze
Fernando Zegers-Hochschild
Maria do Carmo B. Souza
Ramon Carreras
Miguel Ángel Checa
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2017
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-016-0217-2

Other articles of this Issue 1/2017

Reproductive Biology and Endocrinology 1/2017 Go to the issue