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ARC Journal of Gynecology and Obstetrics
Volume-2 Issue-1, 2017, Page No: 21-26
DOI: http://dx.doi.org/10.20431/2456-0561.0201005

Ovarian Endometrioma and Infertility

Akmal El-Mazny1,Ahmed Kamel2

Department of Obstetrics and Gynecology, Faculty of Medicine, Cairo University, Egypt.

Citation : Akmal El-Mazny,Ahmed Kamel, "Ovarian Endometrioma and Infertility". ARC Journal of Gynecology and Obstetrics. 2017;2(1):21-26.

Copyright : © 2017 . This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


Abstract:

The core definition of endometriosis is when endometrial glands and stoma are identified outside the uterine cavity. It is estimated to affect 2-10% of women in their reproductive age, and 50% of patients complain of infertility. Ovarian endometrioma is a common yet a specific presentation of the disease. This review discusses the effect of ovarian endometrioma on fertility and its management.

Keywords: Ovarian endometrioma, Infertility, Ovarian cystectomy, IVF,Gynecology,Obstetrics


1. Introduction

Ovarian endometrioma is defined as a cystic formation within the ovary lined by ectopic endometrium [1]. Its incidence is approximately 17% of subfertile women [2]. It is present in 17-44% of patients with endometriosis [3], and it is estimated that 20-40% women undergoing assisted reproductive techniques (ART) have endometriosis [4].

Three main theories exist for the formation of endometrioma. The first being invagination secondary to bleeding of a superficial implant. It may also be formed through invagination secondary to metaplasia of coelomic epithelium in cortical inclusion cysts, and finally endometriotic transformation of functional cysts.

The diagnosis of endometrioma is tricky as it may be asymptomatic, however it may present with dysmenorrhea, dyspareunia, infertility and sometimes adnexal mass [5]. The tumor marker CA-125 can be elevated in the presence of an endometrioma, but not accurate [6]. Newer marker, follistatin, is showing more promise but its value still remains controversial [7-9].

Trans-vaginal ultrasound for the diagnosis of endometrioma has been reported to havea sensitivity range between 84-100%, and a specificity range between 90-100% [10,11]. Endometriomas can have a wide range of appearances on ultrasound, which may vary from an anechoic cyst to a solid appearing mass [5].

Typically in more than 80% of cases, they appear as a thick walled ovarian cyst containing homogenous "ground-glass" content with no internal vascularity[5,12]. Endometriomata maybe unilateral or bilateral; uni-or multilocular,sometimes single or multiple, and usually more commonon the left side [13].


2. Effect Of Ovarian Endometrioma On Fertility

Endometriosis itself causes infertility through [14,15]:

a) Distortion of the pelvic anatomy.
b) Abnormal utero-tubal transport.
c) Altered peritoneal function.
d) Altered humoral and cell mediated immunity.
e) Impaired implantation.
f) Abnormal oocyte and embryo quality.

A meta-analysis has shown that the pregnancy rate was significantly lower compared to women with tubal infertility [2]. This effect seems to be mediated through altered oocyte quality [16]. Pelvic endometriosis may affect oocyte quality perhaps through increased granulosa cell apoptosis [17]. Also cases with endometrioma have fewer oocytes retrieved during in-vitro fertilization (IVF) [2,18].

Newer evidence is emerging that deep ovarian endometriosis alters the local environment through intra-ovarian oxidative damage [19]. Other studies have shown that the spontaneous ovulation rate is significantly lower in the affected ovary [20,21]. A dose-response effect was observed; when only one endometrioma was present the ovulation rate in the affected ovary was 35%, but when an ovary contained two or more cysts, the ovulation rate was only 19% [22].

An ovarian endometrioma tends to be a sentinel marker of more disseminated endometriosis [23]. The reality is that this condition is usually accompanied by other pelvic lesions and adhesions [24]. This combined effect leads to a more severe disease, which is associated with lower fertility rates .


3. Management Of Ovarian Endometrioma

Is surgery always the answer when ovarian endometriomas are diagnosed with ultrasound? This Depends on a variety of factors which include: age, parity, duration of infertility, associated pain, affordability of treatment, and previous ovarian surgery [25].

3.1. Expectant Management
The scan is repeated in in 2-3 months to exclude a functional cyst or a hemorrhagic corpus luteum cyst. These conditions will resolve with time, and given that endometriomas have an average growth rate of approximately 0.5 cm per 6 months, the size of the endometrioma will not be significantly affected [26].

3.2. Medical Treatment
Gonadotropin releasing hormone (GnRH) agonists or danazol shrinks the size of endometriomas 50% [5,27]. A Meta-analysis had shown a fourfold increase in the odds of clinical pregnancy when GnRH agonists were used 3–6 months as pretreatment to IVF in women with endometriosis [28].

Other authors compared pre-surgical medical therapy versus surgery alone [29], ovulation suppression versus placebo [30], and a meta-analysis which included three reviews comparing GnRH agonists versus antagonists [31]. In all cases there was no evidence of a significant difference in effectiveness, and the quality of the evidence was either low or very low.

3.3. Controlled Ovarian Stimulation And Intrauterine Insemination
In 15,000 studied COH-IUI cycles,endometriosis to be an unfavorable predictor of pregnancy [32]. One IVF cycle was found to be more effective than six cycles of COH-IUI [33].

This may be related to more significantly altered tubo-ovarian anatomy [14,34].

3.4. Surgical Intervention
Usually a conservative approach is the best management, however sometimes surgical interference may be needed in the form of aspiration, ablation or cystectomy.

3.4.1. Aspiration
 The rationale behind it is that the endometriotic lining becomes compressed and atrophic. So aspiration will resolve the condition [3].Its advantages include being simple, minimally invasive procedure, and cystectomy for cysts >3 cm carries an increased risk of diminished ovarian reserve after surgery [35].

Its effect on IVF is controversial as both Dicker et al [36] and Suganuma et al [37] reported betterand worse outcomes respectively. However it’s not without risk as surgical intervention, pelvic abscess, and a recurrence rates 83.3% has been reported [35],38-40].

3.4.2. Chemoablation
 In chemoablation the process of sclerotherapy destroys the epithelial lining of the cyst and hereby reduces the recurrence [41,42]. Various sclerosing agents have been tried, including 95% ethanol, methotrexate, tetracycline, and IL-2 [43-45]. The recurrence rate for sclerotherapy varies between 9.1% and 66.7%. There are not enough studies to conclude its further impact on fertility, and there is an increased risk of associated pelvic abscess [46].

3.4.3. Cystectomy
 Whether the approach for the cystectomy was laparotomy or laparoscopic, the procedure carries potential difficulties and complications. Cystectomy often leads to bleeding of the vascular bed in the hilus, which requires meticulous hemostatic control [47].

Many studies showed that after excision there was an increased risk of diminished ovarian reserve[48].

Excision Versus Ablation
In excision of the endometrioma, the cyst wall is incised either with or without the use of electrosurgical or laser energy. Then a combination of scissors (or a monopolar hook) and grasping forceps is used to excise or ‘strip away’ the cyst wall from the underlying cortex.

Ablation on the other hand involves first opening and then draining the endometrioma, or making a window in the wall of the cyst (fenestration), the cyst wall is then destroyed by either electro coagulation, or some form of laser energy is used [49,50].

A Cochrane Review suggested a benefit of excisional surgery over drainage or ablation for achieving spontaneous pregnancy [51,52]. Another one found no evidence of a difference between surgery (aspiration or cystectomy) and expectant management in clinical pregnancy rates prior to ART [31,51].

Hemostasis: Bipolar Electro Coagulation, Harmonic Scalpel Or Suturing?
Electro coagulation was associated with a reduction in ovarian reserve [53,54]. A Meta- analysis showed that Suturing for hemostasis was associated with a more favorable outcome for ovarian reserve than bipolar electro-coagulation [55]. Another study showed that suturing may also reduce postoperative adhesions compared with bipolar surgery [56].

Studies using topical hemostatic agent (gelatine-thrombin matrix) showed good control of minor bleeding at the end of laparoscopic stripping [57,58].

To Remove Or Not To Remove?
This controversial question plagues the minds of gynecologists. A Cochrane review suggested that excision of endometrioma >3 cm led to five fold spontaneous pregnancy rate.

Other meta-analysis and ESHRE Guidelines concluded that there is no significant effect on ovarian response to stimulation and IVF pregnancy rates compared with no treatment [4,31,59].

Pre-And Post-Surgical Interventions
No evidence to support the use of either Pre- or post-surgical medical therapy (Danazol,GnRHa, progestogens, gestrinone, OCPs) for increasing pregnancy rates [29,51,60].

Recurrences Following Surgery
Recurrences are less after excision than ablation [52,61]. Recurrence decreases with increasing age [62,63]. Two out of the three RCTs recommended postoperative use of cyclic OCPs to delay recurrence[64-66].

3.5. In-Vitro Fertilization (IVF)
There are pathophysiological effects on ovary which include a need for increased cumulative doses of FSH medication and the production of fewer follicles following stimulation [5].

During ovum pick up, the puncture by the needle may increase the associated risk of pelvic abscess. The ovaries are often adherent to the posterior surface of the uterus, where they may be out of reach. The bowel loops may also be fixed in the path of the aspiration needle [67,68].

Endometriosis affects oocyte number but not embryo quality or pregnancy rates and outcome, whether or not an endometrioma is present [18]. Endometrioma has adverse effects only on follicle number and oocytes quality [69]. Yang et al [70] showed same results but less total number of embryos and M2 oocytes. Only a single study showed lower embryo quality and implantation rates, in the presence of endometrioma, however pregnancy outcome was also unaffected [71].

Other studies also showed no adverse effect on IVF outcome [14,67,68]. Fernando et al reported that endometriomas increase the rate of preterm birth [72].

Meta-analysis studying medical Interventions prior to IVF comparing GnRH agonist to GnRH antagonist showed that there was improved ovarian response to stimulation, and the number of oocytes retrieved. However there was no difference in clinical pregnancy rates between either protocol [31,51]. Only a meta-analysis by Sallam et al reported more pregnancies with ultra-long GnRH agonist down-regulation, however it only included three trials and there was a lot of heterogeneity in the inclusion criteria of the included studies [28].

Meta-analysis studying surgical interventions prior to IVF have shown that there is no benefit of laparoscopic aspiration, cystectomy, or transvaginal aspiration of endometrioma over expectant management regarding the clinical pregnancy rate [31].


4. Conclusion

Traditional treatments modalities such as cystectomy and ablation increase the rate of spontaneous pregnancy and lower incidence of recurrence after removal. However thereis no improvement in IVF outcomes and they can potentially cause damage to the ovarian reserve. Less invasive newer and combined techniques are being developed that reduce the damage to the ovarian reserve after cystectomy. More research is needed to determine how these procedures affect IVF outcomes.


References

  1. Garrido N, Navarro J, Remohi J, et al. Follicular hormonal environment and embryo quality in women with endometriosis. Hum Reprod Update. 2000;6:67-74.
  2. Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. FertilSteril. 2002;77:1148–1155.
  3. Gonçalves FC, Andres MP, Passman LJ, et al. A systematic review of ultrasonography-guided transvaginal aspiration of recurrent ovarian endometrioma. Int J Gynaecol Obstet. 2016; 134:3-7.
  4. Dunselman GA, Vermeulen N, Becker C, et al; European Society of Human Reproduction and Embryology. ESHRE guideline: management of women with endometriosis. Hum Reprod. 2014; 29: 400-12.
  5. Rombauts L. Ovarian Endometrioma: Surgery and Fertility Preservation. Endometriosis: Science and Practice, First Edition. Edited by Linda C. Giudice, Johannes L.H. Evers and David L. Healy. Blackwell Publishing Ltd. 2012; chapter 47: 473-81.
  6. Bedaiwy MA, Falcone T. Laboratory testing for endometriosis. Clin Chim Acta. 2004;340:41– 56.
  7. Ant Ö, Özakşit G, Güzel Aİ, et al. Clinical significance of serum follistatin levels in the diagnosis of ovarian endometrioma and benign ovarian cysts. Taiwan J Obstet Gynecol. 2015; 54: 236-9.
  8. Florio P, Reis FM, Torres PB, et al. High serum follistatin levels in women with ovarian endometriosis. Hum Reprod. 2009;24: 2600-6.
  9. Rocha AL, Carrarelli P, Novembri R, et al. Altered expression of activin, cripto, and follistatin in the endometrium of women with endometrioma. Fertil Steril. 2011; 95:2241-6.
  10. Eskenazi B, Warner M, Bonsignore L, et al. Validation study of nonsurgical diagnosis of endometriosis. Fertil Steril. 2001; 76: 929-35.
  11. Alcázar JL, Laparte C, Jurado M, et al. The role of transvaginal ultrasonography combined with color velocity imaging and pulsed Doppler in the diagnosis of endometrioma. Fertil Steril. 1997;67: 487-91.
  12. El-Mazny A, Kamel A, Ramadan W, et al. Effect of ovarian endometrioma on uterine and ovarian blood flow in infertile women. Int J Womens Health. 2016; 8: 677-82.
  13. Bazi T, Nader KA, Seoud MA, et al. Lateral distribution of endometriomas as a function of age. Fertil Steril. 2007; 87: 419-21.
  14. Khine YM, Taniguchi F, Tasuku Harada T. Clinical management of endometriosis-associated infertility. Reprod Med Biol. 2016; 15:217-25.
  15. Pfeifer S, Fritz M, Goldberg J, et al. Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: a committee opinion. Fertil Steril. 2012; 98:591-8.
  16. Garrido N, Navarro J, Remohi J, et al. Follicular hormonal environment and embryo quality in women with endometriosis. Hum Reprod Update. 2000;6:67-74.
  17. Nakahara K, Saito H, Saito T, et al. Ovarian fecundity in patients with endometriosis can be estimated by the incidence of apoptotic bodies. Fertil Steril. 1998;69:931-5.
  18. Suzuki T, Izumi SI, Matsubayashi H, et al. Impact of ovarian endometrioma on oocytes and pregnancy outcomein in vitro fertilization. Fertil Steril. 2005;83: 908-13.
  19. Matsuzaki S, Schubert B. Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis. Fertil Steril. 2010; 93: 2431-2.
  20. Horikawa T, Nakagawa K, Ohgi S. The frequency of ovulation from the affected ovary decreases following laparoscopic cystectomy in infertile women with unilateral endometrioma during a natural cycle. J Assist Reprod Genet. 2008; 25: 239-44.
  21. Schubert B, Canis M, Darcha C, et al. Human ovarian tissue from cortex surrounding benign cysts: a model to study ovarian tissue cryopreservation. Hum Reprod. 2005;20:1786-92.
  22. Benaglia L, Somigliana E, Iemmello R, et al. Endometrioma and oocyte retrieval-induced pelvic abscess: a clinical concern or an exceptional complication? Fertil Steril. 2008; 89: 1263-6.
  23. Redwine DB. Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril. 1999; 72: 310-5.
  24. Chapron C, Pietin-Vialle C, Borghese B, et al. Associated ovarian endometrioma is a marker for greater severity of deeply infiltrating endometriosis. Fertil Steril. 2009; 92: 453-7.
  25. Menakaya U, Infante F, Condous G. Consensus on current management of endometriosis. Hum Reprod. 2013; 28:3162-3.
  26. Seracchioli R, Mabrouk M, Frascà C, et al. Long-term cyclic and continuous oral contraceptive therapy and endometrioma recurrence: a randomized controlled trial. Fertil Steril. 2010; 93:52-6.
  27. Rana N, Thomas S, Rotman C, et al. Decrease in the size of ovarian endometriomas during ovarian suppression in stage IV endometriosis. Role of preoperative medical treatment. J Reprod Med. 1996; 41: 384-92.
  28. Sallam HN, Garcia-Velasco JA, Dias S, et al. Long term pituitary down regulation before in vitro fertilisation (IVF) for women with endometriosis. Cochrane Database Syst Rev. 2006, Issue 1.
  29. Furness S, Yap C, Farquhar C, et al. Pre and post-operative medical therapy for endometriosis surgery. Cochrane Database Syst Rev. 2004, Issue 3.
  30. Hughes E, Brown J, Collins JJ, et al. Ovulation suppression for endometriosis. Cochrane Database Syst Rev. 2007; 3:CD000155.
  31. Benschop L, Farquhar C, van der Poel N, et al. Interventions for women with endometrioma prior to assisted reproductive technology. Cochrane Database Syst Rev. 2010; 11:CD008571.
  32. Steures P, van der Steeg JW, Mol BW, et al; CECERM (Collaborative Effort in Clinical Evaluation in Reproductive Medicine). Prediction of an ongoing pregnancy after intrauterine insemination. Fertil Steril. 2004;82:45-51.
  33. Kissler S, Hamscho N, Zangos S, et al. Diminished pregnancy rates in endometriosis due to impaired uterotubal transport assessed by hysterosalpingoscintigraphy. Br J Obstet Gynaecol. 2005;112: 1391-6.
  34. D’Hooghe TM, Denys B, Spiessens C, et al. Is the endometriosis recurrence rate increased after ovarian hyperstimulation? Fertil Steril. 2006;86:283-90.
  35. Chan LY, So WW, Lao TT. Rapid recurrence of endometrioma after transvaginal ultrasound-guided aspiration. Eur J Obstet Gynecol Reprod Biol. 2003;109:196-8.
  36. Dicker D, Goldman JA, Feldberg D, et al. Transvaginal ultrasonic needle-guided aspiration of endometriotic cysts before ovulation induction for in vitro fertilization. J In Vitro Fert Embryo Transf. 1991;8:286-9.
  37. Suganuma N, Wakahara Y, Ishida D, et al. Pretreatment for ovarian endometrial cyst before in vitro fertilization. Gynecol Obstet Invest. 2002; 54: 36-40.
  38. Mittal S, Kumar S, Kumar A, et al. Ultrasound guided aspiration of endometrioma - a new therapeutic modality to improve reproductive outcome. Int J Gynaecol Obstet. 1999; 65: 17-23.
  39. Younis JS, Ezra Y, Laufer N, et al. Late manifestation of pelvic abscess following oocyte retrieval, for in vitro fertilization, in patients with severe endometriosis and ovarian endometriomata. J Assist Reprod Genet. 1997; 14: 343-6.
  40. Zhu W, Tan Z, Fu Z, et al. Repeat transvaginal ultrasound-guided aspiration of ovarian endometrioma in infertile women with endometriosis. Am J Obstet Gynecol. 2011; 204:61.e1-6.
  41. Chang MY, Hsieh CL, Shiau CS, et al. Ultrasound-guided aspiration and ethanol sclerotherapy (EST) for treatment of cyst recurrence in patients after previous endometriosis surgery: analysis of influencing factors using a decision tree. J Minim Invasive Gynecol. 2013; 20:595-603.
  42. Hsieh CL, Shiau CS, Lo LM, et al. Effectiveness of ultrasound-guided aspiration and sclerotherapy with 95% ethanol for treatment of recurrent ovarian endometriomas. Fertil Steril. 2009;91:2709-13.
  43. García-Tejedor A, Castellarnau M, Ponce J, et al. Ethanol sclerotherapy of ovarian endometrioma: a safe and effective minimal invasive procedure. Preliminary results. Eur J Obstet Gynecol Reprod Biol. 2015;187:25-9.
  44. Acién P, Quereda FJ, Gómez-Torres MJ, et al. GnRH analogues, transvaginal ultrasound-guided drainage and intracystic injection of recombinant interleukin-2 in the treatment of endometriosis. Gynecol Obstet Invest. 2003; 55:96-104.
  45. Agostini A, De Lapparent T, Collette E, et al. In situ methotrexate injection for treatment of recurrent endometriotic cysts. Eur J Obstet Gynecol Reprod Biol. 2007; 130: 129-31.
  46. Mikamo H, Kawazoe K, Sato Y, et al. Ovarian abscess caused by Peptostreptococcusmagnus following transvaginal ultrasound-guided aspiration of ovarian endometrioma and fixation with pure ethanol. Infect Dis Obstet Gynecol. 1998; 6:66-8.
  47. MehdizadehKashi A, Chaichian S, Ariana S, et al. The impact of laparoscopic cystectomy on ovarian reserve in patients with unilateral and bilateral endometrioma. Int J Gynaecol Obstet. 2017; 136: 200-4.
  48. Benaglia L, Somigliana E, Vighi V, et al. Rate of severe ovarian damage following surgery for endometriomas. Hum Reprod. 2010;25: 678-82.
  49. Reich H, Abrao MS. Post-surgical ovarian failure after laparoscopic excision of bilateral endometriomas: is this rare problem preventable? Am J Obstet Gynecol. 2006; 195: 339.
  50. Jones KD, Sutton CJ. Laparoscopic management of ovarian endometriomata: a critical review of current practice. Current Opinion in Obstetrics & Gynecology. 2000; 12:309-15.
  51. Brown J, Farquhar C. Endometriosis: an overview of Cochrane Reviews. Cochrane Database Syst Rev. 2014; 3:CD009590.
  52. Hart RJ, Hickey M, Maouris P, et al. Excisional surgery versus ablative surgery for ovarian endometriomata. Cochrane Database Syst Rev. 2008; 2:CD004992.
  53. Zhang CH, Wu L, Li PQ. Clinical study of the impact on ovarian reserve by different hemostasis methods in laparoscopic cystectomy for ovarian endometrioma. Taiwan J Obstet Gynecol. 2016; 55:507-11.
  54. Li CZ, Liu B, Wen ZQ, et al. The impact of electrocoagulation on ovarian reserve after laparoscopic excision of ovarian cysts: a prospective clinical study of 191 patients. Fertil Steril. 2009;92: 1428-35.
  55. Ding W, Li M, Teng Y. The impact on ovarian reserve of haemostasis by bipolar coagulation versus suture following surgical stripping of ovarian endometrioma: a meta-analysis. Reprod Biomed Online. 2015; 30:635-42.
  56. Pellicano M, Bramante S, Guida M, et al. Ovarian endometrioma: postoperative adhesions following bipolar coagulation and suture. Fertil Steril. 2008; 89:796-9.
  57. Angioli R, Muzii L, Montera R, et al. Feasibility of the use of novel matrix hemostatic sealant (FloSeal) to achieve hemostasis during laparoscopic excision of endometrioma. J Minim Invasive Gynecol. 2009; 16: 153-6.
  58. Ebert AD, Hollauer A, Fuhr N, et al. Laparoscopic ovarian cystectomy without bipolar coagulation or sutures using a gelantine-thrombin matrix sealant (FloSeal): first support of a promising technique. Arch Gynecol Obstet. 2009; 280: 161-5.
  59. Tsoumpou I, Kyrgiou M, Gelbaya TA, et al. The effect of surgical treatment for endometrioma on in vitro fertilization outcomes: a systematic review and meta-analysis. Fertil Steril. 2009; 92:75-87.
  60. Lu D, Song H, Li Y, et al. Pentoxifylline for endometriosis. Cochrane Database Syst Rev. 2012, Issue 1.
  61. Duffy JMN, Arambage K, Correa FJS, Olive D, Fincher S, Garry R, et al. Laparoscopic surgery for endometriosis. Cochrane Database Syst Rev. 2014, Issue 4.
  62. Seo JW, Lee DY, Yoon BK, et al. The age-related recurrence of endometrioma after conservative surgery. Eur J Obstet Gynecol Reprod Biol. 2017; 208: 81-5.
  63. Sengoku K, Miyamoto T, Horikawa M, et al. Clinicopathologic risk factors for recurrence of ovarian endometrioma following laparoscopic cystectomy. Acta Obstet Gynecol Scand. 2013; 92:278-84.
  64. Seracchioli R, Mabrouk M, Frascà C, et al. Long-term cyclic and continuous oral contraceptive therapy and endometrioma recurrence: a randomized controlled trial. Fertil Steril. 2010;93: 52-6.
  65. Sesti F, Capozzolo T, Pietropolli A, et al. Recurrence rate of endometrioma after laparoscopic cystectomy: a comparative randomized trial between post-operative hormonal suppression treatment or dietary therapy vs. placebo. Eur J Obstet Gynecol Reprod Biol. 2009;147: 72-7.
  66. Muzii L, Marana R, Caruana P, et al. Postoperative administration of monophasic combined oral contraceptives after laparoscopic treatment of ovarian endometriomas: a prospective, randomized trial. Am J Obstet Gynecol. 2000; 183: 588-92.
  67. Garcia-Velasco JA, Mahutte NG, Corona J, et al. Removal of endometriomas before in vitro fertilization does not improve fertility outcomes: a matched, case-control study. Fertil Steril. 2004; 81: 1194-7.
  68. Al-Azemi M, Bernal AL, Steele J, et al. Ovarian response to repeated controlled stimulation in in-vitro fertilization cycles in patients with ovarian endometriosis. Hum Reprod. 2000; 15: 72-5.
  69. Gupta S, Agarwal A, Agarwal R, et al. Impact of ovarian endometrioma on assisted reproduction outcomes. Reprod Biomed Online. 2006; 13:349-60.
  70. Yang C, Geng Y, Li Y, et al. Impact of ovarian endometrioma on ovarian responsiveness and IVF: a systematic review and meta-analysis. Reprod Biomed Online. 2015; 31:9-19.
  71. Kumbak B, Kahraman S, Karlikaya G, et al. In vitro fertilization in normoresponder patients with endometriomas: comparison with basal simple ovarian cysts. Gynecol Obstet Invest. 2008; 65: 212-6.
  72. Fernando S, Breheny S, Jaques AM, et al. Preterm birth, ovarian endometriomata, and assisted reproduction technologies. Fertil Steril. 2009; 91: 325-30.

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