Role of surgery in endometriosis-associated subfertility

Analysis of published series reveals that no more than a fourth of subfertile patients undergoing surgery for peritoneal endometriotic implants, rectovaginal endometriotic lesions, or recurrent endometriomas achieved conception spontaneously. First-line surgery for ovarian endometriotic cysts appears associated with a better reproductive performance, that is, a mean postoperative pregnancy rate of ∼50%. At the same time, excision of endometriomas paradoxically seems to induce gonadal damage. With the exception of peritoneal disease, no randomized trials are available to assess the effect of surgery in subfertile women with endometriosis. Therefore, it is not possible to define the absolute benefit increase of the treatment of ovarian and rectovaginal lesions. The decision to undergo surgery for endometriosis-associated subfertility must be shared with the woman after detailed information and taking into account several additional conditions, such as presence of pain, large or complex adnexal masses, bowel or ureteral stenosis, and coexisting infertility factors. When considering surgery, a therapeutic equipoise should be reached that includes demonstrated benefits, potential morbidity, and costs of treatment alternatives. Particularly in case of recurrent endometriosis, in vitro fertilization should generally be preferred to surgery. The role of surgery in endometriosis-associated subfertility includes temporary pain relief in symptomatic women desiring a spontaneous conception. -

- 1 Missmer SA, Hankinson SE, Spiegelman D, Barbieri RL, Marshall LM, Hunter DJ. Incidence of laparoscopically confirmed endometriosis by demographic, anthropometric, and lifestyle factors. Am J Epidemiol 2004; 160 (8) 784-796 - 2 Duignan NM, Jordan JA, Coughlan BM, Logan-Edwards R. One thousand consecutive cases of diagnostic laparoscopy. J Obstet Gynaecol Br Commonw 1972; 79 (11) 1016-1024 - 3 Williams TJ, Pratt JH. Endometriosis in 1,000 consecutive celiotomies: incidence and management. Am J Obstet Gynecol 1977; 129 (3) 245-250 - 4 Strathy JH, Molgaard CA, Coulam CB, Melton III LJ. Endometriosis and infertility: a laparoscopic study of endometriosis among fertile and infertile women. Fertil Steril 1982; 38 (6) 667-672 - 5 Kirshon B, Poindexter III AN. Contraception: a risk factor for endometriosis. Obstet Gynecol 1988; 71 (6 Pt 1) 829-831 - 6 Mahmood TA, Templeton A. Prevalence and genesis of endometriosis. Hum Reprod 1991; 6 (4) 544-549 - 7 Sangi-Haghpeykar H, Poindexter III AN. Epidemiology of endometriosis among parous women. Obstet Gynecol 1995; 85 (6) 983-992 - 8 Hughes EG, Fedorkow DM, Collins JA. A quantitative overview of controlled trials in endometriosis-associated infertility. Fertil Steril 1993; 59 (5) 963-970 - 9 Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: a committee opinion. Fertil Steril 2012; 98 (3) 591-598 - 10 Chandra A, Mosher WD. The demography of infertility and the use of medical care for infertility. Infertil Reprod Med Clin North Am 1994; 5: 283-296 - 11 Schwartz D, Mayaux MJ. Female fecundity as a function of age: results of artificial insemination in 2193 nulliparous women with azoospermic husbands. Federation CECOS. N Engl J Med 1982; 306 (7) 404-406 - 12 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 (10) 2679-2685 - 13 Guzick DS, Silliman NP, Adamson GD , et al. Prediction of pregnancy in infertile women based on the American Society for Reproductive Medicine's revised classification of endometriosis. Fertil Steril 1997; 67 (5) 822-829 - 14 de Ziegler D, Borghese B, Chapron C. Endometriosis and infertility: pathophysiology and management. Lancet 2010; 376 (9742) 730-738 - 15 D'Hooghe TM, Debrock S, Hill JA, Meuleman C. Endometriosis and subfertility: is the relationship resolved?. Semin Reprod Med 2003; 21 (2) 243-254 - 16 Taylor RN, Lebovic DI. Endometriosis. In: Strauss JF, Barbieri R, , eds. Yen and Jaffe's Reproductive Endocrinology: Physiology and Clinical Management. 6th ed. New York, NY: Elsevier; 2009: 577-595 - 17 Marcoux S, Maheux R, Bérubé S. Canadian Collaborative Group on Endometriosis. Laparoscopic surgery in infertile women with minimal or mild endometriosis. N Engl J Med 1997; 337 (4) 217-222 - 18 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 (5) 1332-1334 - 19 Tulandi T, al-Took S. Reproductive outcome after treatment of mild endometriosis with laparoscopic excision and electrocoagulation. Fertil Steril 1998; 69 (2) 229-231 - 20 Wright J, Lotfallah H, Jones K, Lovell D. A randomized trial of excision versus ablation for mild endometriosis. Fertil Steril 2005; 83 (6) 1830-1836 - 21 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 - 22 Broekmans FJ, Kwee J, Hendriks DJ, Mol BW, Lambalk CB. A systematic review of tests predicting ovarian reserve and IVF outcome. Hum Reprod Update 2006; 12 (6) 685-718 - 23 Moore J, Copley S, Morris J, Lindsell D, Golding S, Kennedy S. A systematic review of the accuracy of ultrasound in the diagnosis of endometriosis. Ultrasound Obstet Gynecol 2002; 20 (6) 630-634 - 24 Eskenazi B, Warner M, Bonsignore L, Olive D, Samuels S, Vercellini P. Validation study of nonsurgical diagnosis of endometriosis. Fertil Steril 2001; 76 (5) 929-935 - 25 Ferrazzi E, Zanetta G, Dordoni D, Berlanda N, Mezzopane R, Lissoni AA. Transvaginal ultrasonographic characterization of ovarian masses: comparison of five scoring systems in a multicenter study. Ultrasound Obstet Gynecol 1997; 10 (3) 192-197 - 26 Marrs RP. The use of potassium-titanyl-phosphate laser for laparoscopic removal of ovarian endometrioma. Am J Obstet Gynecol 1991; 164 (6 Pt 1) 1622-1626; discussion 1626–1628 - 27 Beretta P, Franchi M, Ghezzi F, Busacca M, Zupi E, Bolis P. Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation. Fertil Steril 1998; 70 (6) 1176-1180 - 28 Vercellini P, Somigliana E, Viganò P, Abbiati A, Barbara G, Crosignani PG. Surgery for endometriosis-associated infertility: a pragmatic approach. Hum Reprod 2009; 24 (2) 254-269 - 29 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 (2) 179-185 - 30 Busacca M, Riparini J, Somigliana E , et al. Postsurgical ovarian failure after laparoscopic excision of bilateral endometriomas. Am J Obstet Gynecol 2006; 195 (2) 421-425 - 31 Di Prospero F, Micucci G. Is operative laparoscopy safe in ovarian endometriosis?. Reprod Biomed Online 2009; 18 (2) 167 - 32 Benaglia L, Somigliana E, Vighi V, Ragni G, Vercellini P, Fedele L. Rate of severe ovarian damage following surgery for endometriomas. Hum Reprod 2010; 25 (3) 678-682 - 33 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. 03) S238-S242 - 34 Almog B, Shehata F, Sheizaf B, Tan SL, Tulandi T. Effects of ovarian endometrioma on the number of oocytes retrieved for in vitro fertilization. Fertil Steril 2011; 95 (2) 525-527 - 35 Benaglia L, Pasin R, Somigliana E, Vercellini P, Ragni G, Fedele L. Unoperated ovarian endometriomas and responsiveness to hyperstimulation. Hum Reprod 2011; 26 (6) 1356-1361 - 36 Tsolakidis D, Pados G, Vavilis D , et al. The impact on ovarian reserve after laparoscopic ovarian cystectomy versus three-stage management in patients with endometriomas: a prospective randomized study. Fertil Steril 2010; 94 (1) 71-77 - 37 Beretta P, Franchi M, Ghezzi F, Busacca M, Zupi E, Bolis P. Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation. Fertil Steril 1998; 70 (6) 1176-1180 - 38 Alborzi S, Momtahan M, Parsanezhad ME, Dehbashi S, Zolghadri J. A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas. Fertil Steril 2004; 82 (6) 1633-1637 - 39 Hart RJ, Hickey M, Maouris P, Buckett W. Excisional surgery versus ablative surgery for ovarian endometriomata. Cochrane Database Syst Rev 2008; 2 (2) CD004992 - 40 Donnez J, Lousse JC, Jadoul P, Donnez O, Squifflet J. Laparoscopic management of endometriomas using a combined technique of excisional (cystectomy) and ablative surgery. Fertil Steril 2010; 94 (1) 28-32 - 41 Fedele L, Bianchi S, Zanconato G, Bergamini V, Berlanda N. Bipolar electrocoagulation versus suture of solitary ovary after laparoscopic excision of ovarian endometriomas. J Am Assoc Gynecol Laparosc 2004; 11 (3) 344-347 - 42 Kennedy S, Bergqvist A, Chapron C , et al; ESHRE Special Interest Group for Endometriosis and Endometrium Guideline Development Group. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod 2005; 20 (10) 2698-2704 - 43 Vercellini P, Barbara G, Buggio L, Frattaruolo MP, Somigliana E, Fedele L. Effect of patient selection on estimate of reproductive success after surgery for rectovaginal endometriosis: literature review. Reprod Biomed Online 2012; 24 (4) 389-395 - 44 Somigliana E, Infantino M, Candiani M , et al. Association rate between deep peritoneal endometriosis and other forms of the disease: pathogenetic implications. Hum Reprod 2004; 19 (1) 168-171 - 45 Berlanda N, Vercellini P, Fedele L. Rectovaginal or bowel endometriosis. In: Basow DS, , ed. UpToDate. Waltham, MA: UpToDate; 2012. . Available at: Accessed August 21, 2012 - 46 Hudelist G, English J, Thomas AE, Tinelli A, Singer CF, Keckstein J. Diagnostic accuracy of transvaginal ultrasound for non-invasive diagnosis of bowel endometriosis: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2011; 37 (3) 257-263 - 47 Bazot M, Lafont C, Rouzier R, Roseau G, Thomassin-Naggara I, Daraï E. Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis. Fertil Steril 2009; 92 (6) 1825-1833 - 48 Piketty M, Chopin N, Dousset B , et al. Preoperative work-up for patients with deeply infiltrating endometriosis: transvaginal ultrasonography must definitely be the first-line imaging examination. Hum Reprod 2009; 24 (3) 602-607 - 49 Goncalves MO, Podgaec S, Dias Jr JA, Gonzalez M, Abrao MS. Transvaginal ultrasonography with bowel preparation is able to predict the number of lesions and rectosigmoid layers affected in cases of deep endometriosis, defining surgical strategy. Hum Reprod 2010; 25 (3) 665-671 - 50 Vercellini P, Pietropaolo G, De Giorgi O, Daguati R, Pasin R, Crosignani PG. Reproductive performance in infertile women with rectovaginal endometriosis: is surgery worthwhile?. Am J Obstet Gynecol 2006; 195 (5) 1303-1310 - 51 Meuleman C, Tomassetti C, D'Hoore A , et al. Surgical treatment of deeply infiltrating endometriosis with colorectal involvement. Hum Reprod Update 2011; 17 (3) 311-326 - 52 Douay-Hauser N, Yazbeck C, Walker F, Luton D, Madelenat P, Koskas M. Infertile women with deep and intraperitoneal endometriosis: comparison of fertility outcome according to the extent of surgery. J Minim Invasive Gynecol 2011; 18 (5) 622-628 - 53 Bianchi PH, Pereira RM, Zanatta A, Alegretti JR, Motta EL, Serafini PC. Extensive excision of deep infiltrative endometriosis before in vitro fertilization significantly improves pregnancy rates. J Minim Invasive Gynecol 2009; 16 (2) 174-180 - 54 Donnez J, Squifflet J. Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules. Hum Reprod 2010; 25 (8) 1949-1958 - 55 Schonman R, De Cicco C, Corona R, Soriano D, Koninckx PR. Accident analysis: factors contributing to a ureteric injury during deep endometriosis surgery. BJOG 2008; 115 (13) 1611-1615; discussion 1615 - 56 De Cicco C, Corona R, Schonman R, Mailova K, Ussia A, Koninckx P. Bowel resection for deep endometriosis: a systematic review. BJOG 2011; 118 (3) 285-291 - 57 Kondo W, Bourdel N, Tamburro S , et al. Complications after surgery for deeply infiltrating pelvic endometriosis. BJOG 2011; 118 (3) 292-298 - 58 Davey AK, Maher PJ. Surgical adhesions: a timely update, a great challenge for the future. J Minim Invasive Gynecol 2007; 14 (1) 15-22 - 59 Schenken RS, Asch RH, Williams RF, Hodgen GD. Etiology of infertility in monkeys with endometriosis: luteinized unruptured follicles, luteal phase defects, pelvic adhesions, and spontaneous abortions. Fertil Steril 1984; 41 (1) 122-130 - 60 Tulandi T. Salpingo-ovariolysis: a comparison between laser surgery and electrosurgery. Fertil Steril 1986; 45 (4) 489-491 - 61 Frantzen C, Schlösser HW. Microsurgery and postinfectious tubal infertility. Fertil Steril 1982; 38 (4) 397-420 - 62 Caspi E, Halperin Y, Bukovsky I. The importance of periadnexal adhesions in tubal reconstructive surgery for infertility. Fertil Steril 1979; 31 (3) 296-300 - 63 Diamond E. Lysis of postoperative pelvic adhesions in infertility. Fertil Steril 1979; 31 (3) 287-295 - 64 Alborzi S, Motazedian S, Parsanezhad ME. Chance of adhesion formation after laparoscopic salpingo-ovariolysis: is there a place for second-look laparoscopy?. J Am Assoc Gynecol Laparosc 2003; 10 (2) 172-176 - 65 Hammoud A, Gago LA, Diamond MP. Adhesions in patients with chronic pelvic pain: a role for adhesiolysis?. Fertil Steril 2004; 82 (6) 1483-1491 - 66 Howard FM. The role of laparoscopy in the chronic pelvic pain patient. Clin Obstet Gynecol 2003; 46 (4) 749-766 - 67 Robertson D, Lefebvre G, Leyland N , et al; Society of Obstetricians and Gynaecologists of Canada. Adhesion prevention in gynaecological surgery. J Obstet Gynaecol Can 2010; 32 (6) 598-608 - 68 Poncelet C, Ducarme G, Yazbeck C, Madelenat P, Carbonnel M. Safety of transient abdominal ovariopexy in patients with severe endometriosis. Int J Gynaecol Obstet 2012; 118 (2) 120-122 - 69 Daraï E, Touboul C, Ballester M, Poncelet C. Can ovariopexy at the end of surgery for endometriosis be recommended? A case report. J Reprod Med 2012; 57 (1–2) 81-84 - 70 Cheong Y, Tay P, Luk F, Gan HC, Li TC, Cooke I. Laparoscopic surgery for endometriosis: how often do we need to re-operate?. J Obstet Gynaecol 2008; 28 (1) 82-85 - 71 Shakiba K, Bena JF, McGill KM, Minger J, Falcone T. Surgical treatment of endometriosis: a 7-year follow-up on the requirement for further surgery. Obstet Gynecol 2008; 111 (6) 1285-1292 - 72 ISTAT [Istituto Nazionale di Statistica]. Tavole di Fecondita'Regionale [ISTAT, National Institute for Statistics. RegionalFertility Tables]. Available at: Accessed August 19, 2012 - 73 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 (4) 1253-1255 - 74 Evers JL, Dunselman GA, Land JA, Bouckaert PX. Is there a solution for recurrent endometriosis?. Br J Clin Pract Suppl 1991; 72: 45-50; discussion 51–53 - 75 DeCherney AH. Endometriosis: recurrence and retreatment. Clin Ther 1992; 14 (6) 766-772; discussion 765 - 76 Guo SW. Recurrence of endometriosis and its control. Hum Reprod Update 2009; 15 (4) 441-461 - 77 Tandoi I, Somigliana E, Riparini J, Ronzoni S, Vigano' P, Candiani M. High rate of endometriosis recurrence in young women. J Pediatr Adolesc Gynecol 2011; 24 (6) 376-379 - 78 Somigliana E, Vercellini P, Viganó P, Ragni G, Crosignani PG. Should endometriomas be treated before IVF-ICSI cycles?. Hum Reprod Update 2006; 12 (1) 57-64 - 79 Vercellini P, Somigliana E, Viganò P, De Matteis S, Barbara G, Fedele L. The effect of second-line surgery on reproductive performance of women with recurrent endometriosis: a systematic review. Acta Obstet Gynecol Scand 2009; 88 (10) 1074-1082 - 80 Evers LH, Dunselman GA, Land JA, Bouckaert PX. Endometriosis: prevention of recurrences. In: Kempers RD, Cohen J, Haney AF, Younger JB, , eds. Fertility and Reproductive Medicine. Amsterdam, The Netherlands: Excerpta Medica; 1998: 387-396 - 81 Fedele L, Bianchi S, Zanconato G, Berlanda N, Raffaelli R, Fontana E. Laparoscopic excision of recurrent endometriomas: long-term outcome and comparison with primary surgery. Fertil Steril 2006; 85 (3) 694-699 - 82 Cheewadhanaraks S. Comparison of fecundity after second laparotomy for endometriosis to in vitro fertilization and embryo transfer. J Med Assoc Thai 2004; 87 (4) 361-366 - 83 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 fertilization-embryo transfer. Fertil Steril 1996; 65 (4) 791-795 - 84 Busacca M, Chiaffarino F, Candiani M , et al. Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis. Am J Obstet Gynecol 2006; 195 (2) 426-432 - 85 Vercellini P, Parazzini F, Pietropaolo G, Cipriani S, Frattaruolo MP, Fedele L. Pregnancy outcome in women with peritoneal, ovarian and rectovaginal endometriosis: a retrospective cohort study. BJOG 2012; 119 (12) 1538-1543 - 86 Brosens I, Brosens JJ, Fusi L, Al-Sabbagh M, Kuroda K, Benagiano G. Risks of adverse pregnancy outcome in endometriosis. Fertil Steril 2012; 98 (1) 30-35 - 87 Stephansson O, Kieler H, Granath F, Falconer H. Endometriosis, assisted reproduction technology, and risk of adverse pregnancy outcome. Hum Reprod 2009; 24 (9) 2341-2347 - 88 Fedele L, Bianchi S, Zanconato G, Raffaelli R, Berlanda N. Is rectovaginal endometriosis a progressive disease?. Am J Obstet Gynecol 2004; 191 (5) 1539-1542 - 89 Vercellini P, Crosignani PG, Abbiati A, Somigliana E, Viganò P, Fedele L. The effect of surgery for symptomatic endometriosis: the other side of the story. Hum Reprod Update 2009; 15 (2) 177-188 - 90 Berlanda N, Vercellini P, Fedele L. The outcomes of repeat surgery for recurrent symptomatic endometriosis. Curr Opin Obstet Gynecol 2010; 22 (4) 320-325