Influence of endometriosis on assisted reproductive technology outcomes: A systematic review and meta-analysis

Obstetrics and Gynecology

Volumn 125, Issue 1, 2015, Pages 79-88

  Hamdan, Mukhri ^a,b,c,d   Omar, Siti Z ^a,b,c   Dunselman, Gerard ^a,b,c   Cheong, Ying ^a,b,c  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF MALAYA   (Malaysia)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d PRINCESS ANNE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASSISTED REPRODUCTIVE TECHNOLOGY; BIBLIOGRAPHIC DATABASE; DATA SYNTHESIS; ENDOMETRIOSIS; FEMALE; FERTILIZATION IN VITRO; HUMAN; INFERTILITY THERAPY; INTRACYTOPLASMIC SPERM INJECTION; LIVE BIRTH; META ANALYSIS; OBSTETRIC PATIENT; OOCYTE; OUTCOME ASSESSMENT; PREGNANCY RATE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SPONTANEOUS ABORTION; SURGICAL PATIENT; SYSTEMATIC REVIEW; ABORTION, SPONTANEOUS; BIRTH RATE; COHORT ANALYSIS; OOCYTE RETRIEVAL; PREGNANCY; SEVERITY OF ILLNESS INDEX;

ABORTION, SPONTANEOUS; BIRTH RATE; COHORT STUDIES; ENDOMETRIOSIS; FEMALE; FERTILIZATION IN VITRO; HUMANS; LIVE BIRTH; OOCYTE RETRIEVAL; PREGNANCY; RANDOMIZED CONTROLLED TRIALS AS TOPIC; REPRODUCTIVE TECHNIQUES, ASSISTED; SEVERITY OF ILLNESS INDEX;

EID: 84925022748     PISSN: 00297844     EISSN: 1873233X     Source Type: Journal    
DOI: 10.1097/AOG.0000000000000592     Document Type: Review

References (79)

1. Giudice LC, Kao LC. Endometriosis. Lancet 2004;364:1789-99.
2. Holoch KJ, Lessey BA. Endometriosis and infertility. Clin Obstet Gynecol 2010;53:429-38.
3. Farquhar C. Endometriosis. BMJ 2007;334:249-53.
4. Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: A committee opinion. Fertil Steril 2012;98:591-8.
5. Coccia ME, Rizzello F, Mariani G, Bulletti C, Palagiano A, Scarselli G. Impact of endometriosis on in vitro fertilization and embryo transfer cycles in young women: A stage-dependent interference. Acta Obstet Gynecol Scand 2011;90:1232-8.
6. 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;20:3130-5.
7. Lin XN, Wei ML, Tong XM, Xu WH, Zhou F, Huang QX, et al. Outcome of in vitro fertilization in endometriosisassociated infertility: A 5-year database cohort study. Chin Med J (Engl) 2012;125:2688-93.
8. Simon C, Gutiérrez A, Vidal A, de los Santos MJ, Tarin JJ, Remohí J, et al. Outcome of patients with endometriosis in assisted reproduction: results from in-vitro fertilization and oocyte donation. Hum Reprod 1994;9:725-9.
9. Tummon IS, Colwell KA, Mackinnon CJ, Nisker JA, Yuzpe AA. Abbreviated endometriosis-associated infertility correlates with in vitro fertilization success. J In Vitro Fert Embryo Transf 1991;8:149-53.
10. Duffy JM, Arambage K, Correa FJ, Olive D, Farquhar C, Garry R, et al. Laparoscopic surgery for endometriosis. The Cochrane Database of Systematic Reviews 2014, Issue 4. Art. No.: CD011031. DOI: 10.1002/14651858.CD011031.pub2.
11. Parazzini F. Ablation of lesions or no treatment in minimal-mild endometriosis in infertile women: A randomized trial. Gruppo Italiano per lo Studio dell'Endometriosi. Hum Reprod 1999;14: 1332-4.
12. Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil Steril 2002;77:1148-55.
13. Harb H, Gallos I, Chu J, Harb M, Coomarasamy A. The effect of endometriosis on in vitro fertilisation outcome: A systematic review and meta-analysis. BJOG 2013;120:1308-20.
14. National Institute for Health and Care Excellence (NICE). Fertility: Assessment and treatment for people with fertility problems. NICE clinical guideline 156. London (UK): NICE; 2013.
15. European Society of Human Reproduction and Embryology (ESHRE). Management of women with endometriosis. Grimbergen (Belgium): ESHRE; 2013.
16. Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, D'Hooghe T, De Bie B, et al. ESHRE guideline: Management of women with endometriosis. Hum Reprod 2014;29:400-12.
17. Somigliana E, Berlanda N, Benaglia L, Vigano P, Vercellini P, Fedele L. Surgical excision of endometriomas and ovarian reserve: A systematic review on serum antimüllerian hormone level modifications. Fertil Steril 2012;98:1531-8.
18. Carmona F, Chapron C, Martinez-Zamora MÁ, Santulli P, Rabanal A, Martínez-Florensa M, et al. Ovarian endometrioma but not deep infiltrating endometriosis is associated with increased serum levels of interleukin-8 and interleukin-6. J Reprod Immunol 2012;95:80-6.
19. Zegers-Hochschild F, Adamson GD, de Mouzon J, Ishihara O, Mansour R, Nygren K, et al. The International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) Revised Glossary on ART Terminology, 2009. Hum Reprod 2009;24:2683-7.
20. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in metaanalyses. Eur J Epidemiol 2010;25:603-5.
21. Pabuccu R, Onalan G, Kaya C. GnRH agonist and antagonist protocols for stage I-II endometriosis and endometrioma in in vitro fertilization/intracytoplasmic sperm injection cycles. Fertil Steril 2007;88:832-9.
22. Pal L, Shifren JL, Isaacson KB, Chang Y, Leykin L, Toth TL. Impact of varying stages of endometriosis on the outcome of in vitro fertilization-embryo transfer. J Assist Reprod Genet 1998;15:27-31.
23. Chillik CF, Acosta AA, Garcia JE, Perera S, Van Uem JF, Rosenwaks Z, et al. The role of in vitro fertilization in infertile patients with endometriosis. Fertil Steril 1985;44:56-61.
24. Isaacs JD Jr, Hines RS, Sopelak VM, Cowan BD. Ovarian endometriomas do not adversely affect pregnancy success following treatment with in vitro fertilization. J Assist Reprod Genet 1997;14:551-3.
25. Barri PN, Coroleu B, Tur R, Barri-Soldevila PN, Rodríguez I. Endometriosis-associated infertility: Surgery and IVF, a comprehensive therapeutic approach. Reprod Biomed Online 2010;21: 179-85.
26. Esinler I, Bozdag G, Aybar F, Bayar U, Yarali H. Outcome of in vitro fertilization/intracytoplasmic sperm injection after laparoscopic cystectomy for endometriomas. Fertil Steril 2006;85: 1730-5.
27. Matalliotakis I, Cakmak H, Dermitzaki D, Zervoudis S, Goumenou A, Fragouli Y. Increased rate of endometriosis and spontaneous abortion in an in vitro fertilization program: no correlation with epidemiological factors. Gynecol Endocrinol 2008;24:194-8.
28. Yanushpolsky EH, Best CL, Jackson KV, Clarke RN, Barbieri RL, Hornstein MD. Effects of endometriomas on oocyte quality, embryo quality, and pregnancy rates in in vitro fertilization cycles: A prospective, case-controlled study. J Assist Reprod Genet 1998;15:193-7.
29. Azem F, Lessing JB, Geva E, Shahar A, Lerner-Geva L, Yovel I, et al. Patients with stages III and IV endometriosis have a poorer outcome of in vitro fertilization-embryo transfer than patients with tubal infertility. Fertil Steril 1999;72:1107-9.
30. Omland AK, Abyholm T, Fedorcsák P, Ertzeid G, Oldereid NB, Bjercke S, et al. Pregnancy outcome after IVF and ICSI in unexplained, endometriosis-associated and tubal factor infertility. Hum Reprod 2005;20:722-7.
31. Omland AK, Bjercke S, Ertzeid G, Fedorcsák P, Oldereid NB, Storeng R, et al. Intracytoplasmic sperm injection (ICSI) in unexplained and stage I endometriosis-associated infertility after fertilization failure with in vitro fertilization (IVF). J Assist Reprod Genet 2006;23:351-7.
32. Omland AK, Fedorcsák P, Storeng R, Dale PO, Abyholm T, Tanbo T. Natural cycle IVF in unexplained, endometriosisassociated and tubal factor infertility. Hum Reprod 2001;16: 2587-92.
33. Cahill DJ, Wardle PG, Harlow CR, Hull MG. Effect of progestogen therapy on follicular development, related hormone concentrations and fertilization in vitro in unstimulated cycles and unexplained and endometriosis-associated infertility. Hum Reprod 1996;11:647-50.
34. Curtis P, Jackson A, Bernard A, Shaw RW. Pretreatment with gonadotrophin releasing hormone (GnRH) analogue prior to in vitro fertilisation for patients with endometriosis. Eur J Obstet Gynecol Reprod Biol 1993;52:211-6.
35. Díaz I, Navarro J, Blasco L, Simón C, Pellicer A, Remohí J. Impact of stage III-IV endometriosis on recipients of sibling oocytes: Matched case-control study. Fertil Steril 2000;74:31-4.
36. Sung L, Mukherjee T, Takeshige T, Bustillo M, Copperman AB. Endometriosis is not detrimental to embryo implantation in oocyte recipients. J Assist Reprod Genet 1997; 14:152-6.
37. Aboulghar MA, Mansour RT, Serour GI, Al-Inany HG, Aboulghar MM. The outcome of in vitro fertilization in advanced endometriosis with previous surgery: A casecontrolled study. Am J Obstet Gynecol 2003;188:371-5.
38. Mekaru K, Yagi C, Asato K, Masamoto H, Sakumoto K, Aoki Y. Effects of early endometriosis on IVF-ET outcomes. Front Biosci (Elife Ed) 2013;5:720-4.
39. Inoue M, Kobayashi Y, Honda I, Awaji H, Fujii A. The impact of endometriosis on the reproductive outcome of infertile patients. Am J Obstet Gynecol 1992;167:278-82.
40. Pagidas K, Falcone T, Hemmings R, Miron P. Comparison of reoperation for moderate (stage III) and severe (stage IV) endometriosis-related infertility with in vitro fertilizationembryo transfer. Fertil Steril 1996;65:791-5.
41. 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;97:912-8.
42. Al-Fadhli R, Kelly SM, Tulandi T, Tanr SL. Effects of different stages of endometriosis on the outcome of in vitro fertilization. J Obstet Gynaecol Can 2006;28:888-91.
43. Loo TC, Lin MY, Chen SH, Chung MT, Tang HH, Lin LY, et al. Endometrioma undergoing laparoscopic ovarian cystectomy: Its influence on the outcome of in vitro fertilization and embryo transfer (IVF-ET). J Assist Reprod Genet 2005; 22:329-33.
44. Kuroda K. The impact of endometriosis, endometrioma and ovarian cystectomy on assisted reproductive technology. Reprod Med Online 2009;8:113-8.
45. Dong X, Liao X, Wang R, Zhang H. The impact of endometriosis on IVF/ICSI outcomes. Int J Clin Exp Pathol 2013;6:1911-8.
46. Olivennes F, Feldberg D, Liu HC, Cohen J, Moy F, Rosenwaks Z. Endometriosis: A stage by stage analysis-the role of in vitro fertilization. Fertil Steril 1995;64:392-8.
47. May J, Gemmell J, Crawford J, Lyall H. Outcome of IVF/ICSI referrals from the Royal Alexandra Hospital (level 2 infertility service) to Glasgow Royal Infirmary (level 3 infertility service). J Obstet Gynaecol 2012;32:566-8.
48. Kim CH, Ahn JW, Kim SH, Chae HD, Kang BM. Effects on in vitro fertilization-embryo transfer outcomes of vascular endothelial growth factor receptor-1, -2 and -3 in eutopic endometrial tissue of women with endometriosis. J Obstet Gynaecol Res 2011;37:1631-7.
49. Mohamed AM, Chouliaras S, Jones CJ, Nardo LG. Live birth rate in fresh and frozen embryo transfer cycles in women with endometriosis. Eur J Obstet Gynecol Reprod Biol 2011;156: 177-80.
50. Falconer H, Sundqvist J, Gemzell-Danielsson K, von Schoultz B, D'Hooghe TM, Fried G. IVF outcome in women with endometriosis in relation to tumour necrosis factor and anti-Müllerian hormone. Reprod Biomed Online 2009;18: 582-8.
51. Nejad E, Rashidi B, Lardi A, Ezabadi Z, Jahangiri N, Nekoo E. The outcome of in vitro fertilization/intracytoplasmic sperm injection in endometriosis-associated and tubal factor infertility. Iran J Reprod Med 2009;7:1-5.
52. 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;20:3130-5.
53. Hickman TN. Impact of endometriosis on implantation. Data from the Wilford Hall Medical center IVF-ET program. J Reprod Med 2002;47:801-8.
54. Bukulmez O, Yarali H, Gurgan T. The presence and extent of endometriosis do not effect clinical pregnancy and implantation rates in patients undergoing intracytoplasmic sperm injection. Eur J Obstet Gynecol Reprod Biol 2001;96:102-7.
55. Meden-Vrtovec H, Tomazevic T, Verdenik I. Infertility treatment by in vitro fertilization in patients with minimal or mild endometriosis. Clin Exp Obstet Gynecol 2000;27:191-3.
56. Bergendal A, Naffah S, Nagy C, Bergqvist A, Sjoblom P, Hillensjö T. Outcome of IVF in patients with endometriosis in comparison with tubal-factor infertility. J Assist Reprod Genet 1998;15:530-4.
57. Hull MG, Williams JA, Ray B, McLaughlin EA, Akande VA, Ford WC. The contribution of subtle oocyte or sperm dysfunction affecting fertilization in endometriosis-associated or unexplained infertility: A controlled comparison with tubal infertility and use of donor spermatozoa. Hum Reprod 1998;13:1825-30.
58. Pellicer A, Valbuena D, Bauset C, Albert C, Bonilla-Musoles F, Remohi J, et al. The follicular endocrine environment in stimulated cycles of women with endometriosis: Steroid levels and embryo quality. Fertil Steril 1998;69:1135-41.
59. Huang HY, Lee CL, Lai YM, Chang MY, Chang SY, Soong YK. The outcome of in vitro fertilization and embryo transfer therapy in women with endometriosis failing to conceive after laparoscopic conservative surgery. J Am Assoc Gynecol Laparosc 1997;4:299-303.
60. Arici A, Oral E, Bukulmez O, Duleba A, Olive DL, Jones EE. The effect of endometriosis on implantation: results from the Yale University in vitro fertilization and embryo transfer program. Fertil Steril 1996;65:603-7.
61. Tanbo T, Omland A, Dale PO, Abyholm T. In vitro fertilization/embryo transfer in unexplained infertility and minimal peritoneal endometriosis. Acta Obstet Gynecol Scand 1995;74:539-43.
62. Geber S, Paraschos T, Atkinson G, Margara R, Winston RM. Results of IVF in patients with endometriosis: The severity of the disease does not affect outcome, or the incidence of miscarriage. Hum Reprod 1995;10:1507-11.
63. Dmowski WP, Gleicher N. Does endometriosis have an adverse effect on the fertilization in vitro and the IVF outcome? J Assist Reprod Genet 1998;15:527-9.
64. Mills MS, Eddowes HA, Cahill DJ, Fahy UM, Abuzeid MI, McDermott A, et al. A prospective controlled study of in-vitro fertilization, gamete intra-fallopian transfer and intrauterine insemination combined with superovulation. Hum Reprod 1992;7:490-4.
65. Mahmood TA, Arumugam K, Templeton AA. Oocyte and follicular fluid characteristics in women with mild endometriosis. Br J Obstet Gynaecol 1991;98:573-7.
66. Frydman R, Belaisch-Allart JC. Results of in vitro fertilization for endometriosis. Contrib Gynecol Obstet 1987;16:328-36.
67. Matson PL, Yovich JL. The treatment of infertility associated with endometriosis by in vitro fertilization. Fertil Steril 1986;46:432-4.
68. Wardle PG, Mitchell JD, McLaughlin EA, Ray BD, McDermott A, Hull MG. Endometriosis and ovulatory disorder: reduced fertilisation in vitro compared with tubal and unexplained infertility. Lancet 1985;2:236-9.
69. Mahadevan MM, Trounson AO, Leeton JF. The relationship of tubal blockage, infertility of unknown cause, suspected male infertility, and endometriosis to success of in vitro fertilization and embryo transfer. Fertil Steril 1983;40:755-62.
70. Opøien HK, Fedorcsak P, Byholm T, Tanbo T. Complete surgical removal of minimal and mild endometriosis improves outcome of subsequent IVF/ICSI treatment. Reprod Biomed Online 2011;23:389-95.
71. Sharkey AM, Macklon NS. The science of implantation emerges blinking into the light. Reprod Biomed Online 2013; 27:453-60.
72. Gupta S, Goldberg JM, Aziz N, Goldberg E, Krajcir N, Agarwal A. Pathogenic mechanisms in endometriosisassociated infertility. Fertil Steril 2008;90:247-57.
73. Jacobson TZ, Duffy JM, Barlow D, Koninckx PR, Garry R. Laparoscopic surgery for pelvic pain associated with endometriosis. The Cochrane Database of Systematic Reviews 2009, Issue 8. Art. No.: CD001300. DOI: 10.1002/14651858.CD001300.pub3.
74. Kondo W, Bourdel N, Tamburro S, Cavoli D, Jardon K, Rabischong B, et al. Complications after surgery for deeply infiltrating pelvic endometriosis. BJOG 2011;118:292-8.
75. Guyer C. A randomised, single-blind clinical trial to investigate the effectiveness of bipolar versus monopolar diathermy treatment on pain symptoms for women with newly diagnosed superficial endometriosis: The SET study (Superficial Endometriosis Treatment). 2014. Available at: Http://www.controlledtrials.com/ISRCTN37028168/ensdometriosis. Retrieved September 25, 2014.
76. Benschop L, Farquhar C, van der Poel N, Heineman MJ. Interventions for women with endometrioma prior to assisted reproductive technology. The Cochrane Database of Systematic Reviews 2010, Issue 11. Art. No.; CD008571. DOI: 10. 1002/14651858.CD008571.pub2.
77. Tsoumpou I, Kyrgiou M, Gelbaya TA, Nardo LG. The effect of surgical treatment for endometrioma on in vitro fertilization outcomes: A systematic review and meta-analysis. Fertil Steril 2009;92:75-87.
78. Vercellini P, Somigliana E, Viganò P, Abbiati A, Barbara G, Crosignani PG. Surgery for endometriosis-associated infertility: A pragmatic approach. Hum Reprod 2009;24:254-69.
79. Gelbaya TA, Gordts S, D'Hooghe TM, Gergolet M, Nardo LG. Management of endometrioma prior to IVF: compliance with ESHRE guidelines. Reprod Biomed Online 2010;21:325-30.