Aims: Our objective was to predict natural pregnancy after endometriosis surgery using the endometriosis fertility index (EFI). Methods: A retrospective medical records review was conducted, examining patients surgically treated for endometriosis at a single center in Korea between January 2009 and February 2015. In total, 68 women attempting natural conception were analyzed by assessing age, preoperative serum CA-125, body mass index, revised American Fertility Society (rAFS) stage, EFI, and pregnancy outcome. Kaplan-Meier estimates and log-rank tests were used to generate cumulative natural pregnancy rate curves based on an EFI cut-point. A receiver-operating characteristic (ROC) curve was plotted for EFI. Results: Seventy-seven patients attempted conceptions, resulting in 33 natural and 9 assisted conceptions. Excluding assisted conceptions, the mean EFI scores of 68 women who were not pregnant and pregnant were 5.43 ± 0.36 and 6.88 ± 0.28 respectively. The relation between EFI and natural pregnancy was significant (cumulative overall pregnancy rate, p = 0.006), whereas rAFS stage was not (univariate logistics, p = 0.853). The cut-point for maximum natural pregnancy outcomes was 6 (area under ROC curve = 0.710, 95% CI 0.586–0.835). Conclusion: The EFI is a reliable staging system for predicting natural pregnancy after endometriosis surgery. EFI scores can be used to guide postoperative treatment of women with endometriosis.

Keywords:
Endometriosis, Fertility, Endometriosis fertility index, Cumulative pregnancy rate
1.
Zegers-Hochschild F, Adamson GD, Dyer S, Racowsky C, de Mouzon J, Sokol R, Rienzi L, Sunde A, Schmidt L, Cooke ID, Simpson JL, van der Poel S: The international glossary on infertility and fertility care, 2017. Fertil Steril 2017; 108: 393–406.
2.
Practice Committee of the American Society for Reproductive M: Endometriosis and infertility: a committee opinion. Fertil Steril 2012; 98: 591–598.
3.
Revised american society for reproductive medicine classification of endometriosis: 1996. Fertil Steril 1997; 67: 817–821.
4.
Revised american fertility society classification of endometriosis: 1985. Fertil Steril 1985; 43: 351–352.
5.
Jacobson TZ, Duffy JM, Barlow D, Farquhar C, Koninckx PR, Olive D: Laparoscopic surgery for subfertility associated with endometriosis. Cochrane Database Syst Rev 2010; 1: CD001398.
6.
Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, D'Hooghe T, De Bie B, Heikinheimo O, Horne AW, Kiesel L, Nap A, Prentice A, Saridogan E, Soriano D, Nelen W, European Society of Human R, Embryology: Eshre guideline: management of women with endometriosis. Hum Reprod 2014; 29: 400–412.
7.
Marcoux S, Maheux R, Berube S: Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian collaborative group on endometriosis. N Engl J Med 1997; 337: 217–222.
8.
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: 1332–1334.
9.
Palmisano GP, Adamson GD, Lamb EJ: Can staging systems for endometriosis based on anatomic location and lesion type predict pregnancy rates? Int J Fertil Menopausal Stud 1993; 38: 241–249.
10.
Vercellini P, Fedele L, Aimi G, De Giorgi O, Consonni D, Crosignani PG: Reproductive performance, pain recurrence and disease relapse after conservative surgical treatment for endometriosis: the predictive value of the current classification system. Hum Reprod 2006; 21: 2679–2685.
11.
Adamson GD: Endometriosis classification: an update. Curr Opin Obstet Gynecol 2011; 23: 213–220.
12.
Adamson GD, Pasta DJ: Endometriosis fertility index: the new, validated endometriosis staging system. Fertil Steril 2010; 94: 1609–1615.
13.
Garavaglia E, Pagliardini L, Tandoi I, Sigismondi C, Vigano P, Ferrari S, Candiani M: External validation of the endometriosis fertility index (EFI) for predicting spontaneous pregnancy after surgery: further considerations on its validity. Gynecol Obstet Invest 2015; 79: 113–118.
14.
Maheux-Lacroix S, Nesbitt-Hawes E, Deans R, Won H, Budden A, Adamson D, Abbott JA: Endometriosis fertility index predicts live births following surgical resection of moderate and severe endometriosis. Hum Reprod 2017; 32: 2243–2249.
15.
Zegers-Hochschild F, Adamson GD, de Mouzon J, Ishihara O, Mansour R, Nygren K, Sullivan E, Vanderpoel S: International committee for monitoring assisted reproductive technology (ICMART) and the world health organization (WHO) revised glossary of art terminology, 2009. Fertil Steril 2009; 92: 1520–1524.
16.
Bourdel N, Alves J, Pickering G, Ramilo I, Roman H, Canis M: Systematic review of endometriosis pain assessment: how to choose a scale? Hum Reprod Update 2015; 21: 136–152.
17.
Somigliana E, Benaglia L, Vigano P, Candiani M, Vercellini P, Fedele L: Surgical measures for endometriosis-related infertility: a plea for research. Placenta 2011; 32(suppl 3):S238–S242.
18.
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: 217–230.
19.
Vercellini P, Carmignani L, Rubino T, Barbara G, Abbiati A, Fedele L: Surgery for deep endometriosis: a pathogenesis-oriented approach. Gynecol Obstet Invest 2009; 68: 88–103.
20.
Vercellini P, Somigliana E, Daguati R, Barbara G, Abbiati A, Fedele L: The second time around: reproductive performance after repetitive versus primary surgery for endometriosis. Fertil Steril 2009; 92: 1253–1255.
21.
Buggio L, Pagliardini L, Gentilini D, De Braud L, Vigano P, Vercellini P: A rare familial case of endometriosis with very severe gynecological and obstetric complications: novel genetic variants at a glance. Gynecol Obstet Invest 2014; 77: 201–204.
22.
Macer ML, Taylor HS: Endometriosis and infertility: a review of the pathogenesis and treatment of endometriosis-associated infertility. Obstet Gynecol Clin North Am 2012; 39: 535–549.
23.
Tomassetti C, Geysenbergh B, Meuleman C, Timmerman D, Fieuws S, D'Hooghe T: External validation of the endometriosis fertility index (EFI) staging system for predicting non-art pregnancy after endometriosis surgery. Hum Reprod 2013; 28: 1280–1288.
24.
Johnson NP, Hummelshoj L, Adamson GD, Keckstein J, Taylor HS, Abrao MS, Bush D, Kiesel L, Tamimi R, Sharpe-Timms KL, Rombauts L, Giudice LC: World endometriosis society consensus on the classification of endometriosis. Hum Reprod 2017; 32: 315–324.
25.
Boujenah J, Bonneau C, Hugues JN, Sifer C, Poncelet C: External validation of the endometriosis fertility index in a french population. Fertil Steril 2015; 104: 119–123.e111.
26.
Zeng C, Xu JN, Zhou Y, Zhou YF, Zhu SN, Xue Q: Reproductive performance after surgery for endometriosis: Predictive value of the revised american fertility society classification and the endometriosis fertility index. Gynecol Obstet Invest 2014; 77: 180–185.
27.
Brown J, Farquhar C: Endometriosis: an overview of cochrane reviews. Cochrane Database Syst Rev 2014; 3:CD009590.
28.
Talmor A, Dunphy B: Female obesity and infertility. Best Pract Res Clin Obstet Gynaecol 2015; 29: 498–506.
29.
Silvestris E, de Pergola G, Rosania R, Loverro G: Obesity as disruptor of the female fertility. Reprod Biol Endocrinol 2018; 16: 22.
30.
Jungheim ES, Travieso JL, Hopeman MM: Weighing the impact of obesity on female reproductive function and fertility. Nutr Rev 2013; 71(suppl 1):S3–S8.
31.
Liu Y, Zhang W: Association between body mass index and endometriosis risk: a meta-analysis. Oncotarget 2017; 8: 46928–46936.
32.
Vigano P, Somigliana E, Panina P, Rabellotti E, Vercellini P, Candiani M: Principles of phenomics in endometriosis. Hum Reprod Update 2012; 18: 248–259.
33.
Lafay Pillet MC, Schneider A, Borghese B, Santulli P, Souza C, Streuli I, de Ziegler D, Chapron C: Deep infiltrating endometriosis is associated with markedly lower body mass index: a 476 case-control study. Hum Reprod 2012; 27: 265–272.
34.
Practice Committee of the American Society for Reproductive M: Diagnostic evaluation of the infertile male: a committee opinion. Fertil Steril 2015; 103:e18–25.
35.
Practice Committee of the American Society for Reproductive M: Diagnostic evaluation of the infertile female: a committee opinion. Fertil Steril 2015; 103:e44–50.
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2018
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