Prevention of endometriosis
Primary prevention
Primary prevention is defined as those measures that protect healthy individuals from developing the disease. A typical example is immunization against infectious diseases, but it also includes health promotion and regulation of environmental pollutants.
Given that the exact cause and pathogenesis of endometriosis are unknown, potential interventions for primary prevention are limited. In light of the retrograde menstruation theory, the use of COCs for primary prevention has been suggested (105). COCs suppress ovulation and substantially reduce the amount of monthly uterine blood flow. They are successfully used in the treatment of pain symptoms and progestogens may inhibit expression of matrix metalloproteinases and angiogenesis. The relationship between COC use and risk of endometriosis was evaluated in a systematic review by Vercellini and colleagues in 2011 (105). The authors conclude that the risk of endometriosis appears reduced during COC use, but that it is not possible to exclude the possibility that the apparent protective effect of COC against endometriosis is the result of postponement of surgical evaluation due to temporary suppression of pain symptoms (105). Based on this meta-analysis, the ESHRE guideline states that the usefulness of oral contraceptives for the primary prevention of endometriosis is uncertain (2).
A second factor that has been investigated is the possible link between the level of physical activity and endometriosis. Physical activity has been hypothesized to be protective against endometriosis because it may increase levels of sex hormone-binding globulin, which would reduce bioavailable oestrogens, and it reduces insulin resistance and hyperinsulinaemia, which has been hypothesized to be related to endometriosis (106). Several case-control studies reported a strong risk reduction of endometriosis associated with physical activity (107-110).
Based on prospective collected data from the Nurses' Health Study II, Vitonis and colleagues could not replicate these strong associations. They observed a weak protective effect among fertile participants for total recreational physical activity reported 2 years before diagnosis and a slightly stronger protective effect for aerobic exercise on the rate of laparoscopically confirmed endometriosis (106). Based on these prospective data, the ESHRE guideline states that the usefulness of physical exercise for the primary prevention of endometriosis is uncertain (2).Secondary prevention
Secondary preventive measures are those interventions used to prevent recurrences, exacerbations, or complications of the disease and its treatment. In the ESHRE guideline, secondary prevention of endometriosis was defined as prevention of the recurrence of pain symptoms (dysmenorrhea, dyspareunia, non-menstrual pelvic pain) or the recurrence of disease (recurrence of endometriosis lesions documented by ultrasound for ovarian endometrioma or by laparoscopy for all endometriosis lesions) in the long term (more than 6 months after surgery) (2).
A frustrating aspect of surgical treatment of endometriosis is the variable recurrence rate, between 10% and 55% within 12 months after excision/removal by an expert in endometriosis surgery, with an extra 10% of recurrence for each additional year after surgery (111). Logically, there has been significant interest in the effect of pre- and postoperative medical therapies for lowering recurrence and complication rates after surgical treatment of endometriosis. A Cochrane review considered both pre-and postoperative treatment in relation to the management of cysts, pain, and infertility. The authors conclude that there is no evidence of a benefit of preoperative medical therapy on the outcome of surgery (95). The ESHRE guideline endorses that preoperative treatment with GnRH analogues to facilitate surgery is common clinical practice, although there are no controlled studies supporting this (2).
Based on the same Cochrane review, both the ESHRE and ASRM guidelines recommend the use of long-term (>6 months) postoperative hormonal treatment (COC, levonorgestrel-releasing intrauterine device, pro- gestogens) for the secondary prevention of recurrence of both symptoms and lesions (2, 38). It is important to note that postoperative medical treatment does not improve outcome of surgery and as such there is no clear rationale for short- term (of the endometriosis fertility index (EFI) staging system for predicting non-ART pregnancy after endometriosis surgery. Hum Reprod 2013;28:1280-88.36. Tuttlies F, Keckstein J, Ulrich U, et al. [ENZIAN-score, a classification of deep infiltrating endometriosis.] Zentralbl Gynakol 2005;127:275-81.
37. Haas D, Shebl O, Shamiyeh A, Oppelt P. The rASRM score and the Enzian classification for endometriosis: their strengths and weaknesses. Acta Obstet Gynecol Scand 2013;92:3-7.
38. Practice Committee of the American Society for Reproductive Medicine. Treatment of pelvic pain associated with endometriosis: a committee opinion. Fertil Steril 2014;101:927-35.
39. Nisenblat V, Bossuyt PM, Farquhar C, Johnson N, Hull ML. Imaging modalities for the non-invasive diagnosis of endometriosis. Cochrane Database Syst Rev 2016;2:CD009591.
40. Faccioli N1, Foti G, Manfredi R, et al. Barium enema evaluation of colonic involvement in endometriosis. AJR Am J Roentgenol 2008;190:1050-54.
41. Ribeiro HS, Ribeiro PA, Rossini L, Rodrigues FC, Donadio N, Aoki T. Double-contrast barium enema and transrectal endoscopic ultrasonography in the diagnosis of intestinal deeply infiltrating endometriosis. J Minim Invasive Gynecol 2008;15:315-20.
42. Savelli L, Manuzzi L, Coe M, et al. Comparison of transvaginal sonography and double-contrast barium enema for diagnosing deep infiltrating endometriosis of the posterior compartment. Ultrasound Obstet Gynecol 2011;38:466-71.
43. Vanhie A, Meuleman C, Tomassetti C, et al. Consensus on recording deep endometriosis surgery: the CORDES statement.
Hum Reprod 2016;31:1219-23.44. Exacoustos C, Malzoni M, Di Giovanni A, et al. Ultrasound mapping system for the surgical management of deep infiltrating endometriosis. Fertil Steril 2014;102:143-50.e2.
45. Bellelis P, Dias JA Jr, Podgaec S, Gonzales M, Baracat EC, Abrao MS. Epidemiological and clinical aspects of pelvic endometriosis- a case series. Rev Assoc Med Bras 2010;56:467-71.
46. Nnoaham KE, Hummelshoj L, Kennedy SH, et al. Developing symptom-based predictive models of endometriosis as a clinical screening tool: results from a multicenter study. Fertil Steril 2012;98:692-701.e5.
47. Koninckx PR1, Meuleman C, Oosterlynck D, Cornillie FJ. Diagnosis of deep endometriosis by clinical examination during menstruation and plasma CA-125 concentration. Fertil Steril 1996;65:280-87.
48. Bazot M, Lafont C, Rouzier R, et al. Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis. Fertil Steril 2009;92:1825-33.
49. Chapron C, Dubuisson JB, Pansini V, et al. Routine clinical examination is not sufficient for diagnosing and locating deeply infiltrating endometriosis. JAm Assoc Gynecol Laparosc 2002;9:115-19.
50. [No authors listed] Practice bulletin no. 114: management of endometriosis. Obstet Gynecol 2010;116:223-36.
51. Van Holsbeke C, Van Calster B, Guerriero S, et al. Endometriomas: their ultrasound characteristics. Ultrasound Obstet Gynecol 2010;35:730-40.
52. Hudelist G, English J, Thomas AE, Tinelli A, Singer CF, Keckstein J. Diagnostic accuracy of transvaginal ultrasound for non-inva- sive diagnosis of bowel endometriosis: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2011;37:257-63.
53. Redwine DB. Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril 1999;72:310-15.
54. Noventa M, Saccardi C, Litta P, et al. Ultrasound techniques in the diagnosis of deep pelvic endometriosis: algorithm based on a systematic review and meta- analysis.
Fertil Steril 2015;104:366-83.e2.55. Saba L, Sulcis R, Melis GB, et al. Endometriosis: the role of magnetic resonance imaging. Acta Radiol 2015;56:355-67.
56. Kinkel K, Frei KA, Balleyguier C, Chapron C. Diagnosis of endometriosis with imaging: a review. Eur Radiol 2006;16:285-98.
57. Wykes CB, Clark TJ, Khan KS. Accuracy of laparoscopy in the diagnosis of endometriosis: a systematic quantitative review. BJOG 2004;111:1204-12.
58. Clement PB. The pathology of endometriosis: a survey of the many faces of a common disease emphasizing diagnostic pitfalls and unusual and newly appreciated aspects. Adv Anat Pathol 2007;14:241-60.
59. Jenkins TR, Liu CY, White J. Does response to hormonal therapy predict presence or absence of endometriosis? J Minim Invasive Gynecol 2008;15:82-86.
60. Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: a committee opinion. Fertil Steril 2012;98:591-98.
61. Vercellini P, Crosignani P, Somigliana E, Vigano P, Frattaruolo MP, Fedele L. ‘Waiting for Godot’: a commonsense approach to the medical treatment of endometriosis. Hum Reprod 2011;26:3-13.
62. Marjoribanks J, Proctor M, Farquhar C, Derks RS. Nonsteroidal anti-inflammatory drugs for dysmenorrhoea. Cochrane Database Syst Rev 2010;1:CD001751.
63. Allen C, Hopewell S, Prentice A. Nonsteroidal anti-inflammatory drugs for pain in women with endometriosis. Cochrane Database Syst Rev 2009;2:CD004753.
64. Davis L, Kennedy SS, Moore J, Prentice A. Oral contraceptives for pain associated with endometriosis. Cochrane Database Syst Rev 2007;3:CD001019.
65. Meresman GF, Auge L, Baranao RI, Lombardi E, Tesone M, Sueldo C. Oral contraceptives suppress cell proliferation and enhance apoptosis of eutopic endometrial tissue from patients with endometriosis. Fertil Steril 2002;77:1141-47.
66. Vercellini P, Trespidi L, Colombo A, Vendola N, Marchini M, Crosignani PG. A gonadotropin-releasing hormone agonist versus a low-dose oral contraceptive for pelvic pain associated with endometriosis.
Fertil Steril 1993;60:75-79.67. Brown J, Kives S, Akhtar M. Progestagens and anti-progestagens for pain associated with endometriosis. Cochrane Database Syst Rev 2012;3:CD002122.
68. Olive DL. Gonadotropin-releasing hormone agonists for endometriosis. N Engl J Med 2008;359:1136-42.
69. Barbieri RL. Hormone treatment of endometriosis: the estrogen threshold hypothesis. Am J Obstet Gynecol 1992;166:740-45.
70. Brown J, Pan A, Hart RJ. Gonadotrophin-releasing hormone analogues for pain associated with endometriosis. Cochrane Database Syst Rev 2010;12:CD008475.
71. Makarainen L, Ronnberg L, Kauppila A. Medroxyprogesterone acetate supplementation diminishes the hypoestrogenic side effects of gonadotropin-releasing hormone agonist without changing its efficacy in endometriosis. Fertil Steril 1996;65:29-34.
72. Moghissi KS, Schlafll WD, Olive DL, Skinner MA, Yin H. Goserelin acetate (Zoladex) with or without hormone replacement therapy for the treatment of endometriosis. Fertil Steril 1998;69:1056-62.
73. Taskin O, Yalcinoglu AI, Kucuk S, Uryan I, Buhur A, Burak F. Effectiveness of tibolone on hypoestrogenic symptoms induced by goserelin treatment in patients with endometriosis. Fertil Steril 1997;67:40-45.
74. Bergqvist A, Jacobson J, Harris S. A double-blind randomized study of the treatment of endometriosis with nafarelin or nafarelin plus norethisterone. Gynecol Endocrinol 1997;11:187-94.
75. Ferrero S, Venturini PL, Ragni N, Camerini G, Remorgida V. Pharmacological treatment of endometriosis: experience with aromatase inhibitors. Drugs 2009;69:943-52.
76. Ferrero S, Remorgida V, Maganza C, et al. Aromatase and endometriosis: estrogens play a role. Ann N YAcad Sci 2014;1317:17-23.
77. Bulun SE, Fang Z, Imir G, et al. Aromatase and endometriosis. Semin Reprod Med 2004;22:45-50.
78. Ferrero S, Gillott DJ, Venturini PL, Remorgida V. Use of aromatase inhibitors to treat endometriosis-related pain symptoms: a systematic review. Reprod Biol Endocrinol 2011;9:89.
79. Crosignani PG, Vercellini P, Biffignandi F, Costantini W, Cortesi I, Imparato E. Laparoscopy versus laparotomy in conservative surgical treatment for severe endometriosis. Fertil Steril 1996;66:706-11.
80. Duffy JM, Arambage K, Correa FJ, et al. Laparoscopic surgery for endometriosis. Cochrane Database Syst Rev 2014;4:CD011031.
81. Healey M, Ang WC, Cheng C. Surgical treatment of endometriosis: a prospective randomized double-blinded trial comparing excision and ablation. Fertil Steril 2010;94:2536-40.
82. Wright J, Lotfallah H, Jones K, Lovell D. A randomized trial of excision versus ablation for mild endometriosis. Fertil Steril 2005;83:1830-36.
83. Carmona F, Martinez-Zamora MA, Rabanal A, Martinez-Roman S, Balasch J. Ovarian cystectomy versus laser vaporization in the treatment of ovarian endometriomas: a randomized clinical trial with a five-year follow-up. Fertil Steril 2011;96:251-54.
84. Hart RJ, Hickey M, Maouris P, Buckett W Excisional surgery versus ablative surgery for ovarian endometriomata. Cochrane Database Syst Rev 2008;2:CD004992.
85. Raffi F, Metwally M, Amer S. The impact of excision of ovarian endometrioma on ovarian reserve: a systematic review and metaanalysis. J Clin Endocrinol Metab 2012;97:3146-54.
86. Busacca M, Riparini J, Somigliana E, et al. Postsurgical ovarian failure after laparoscopic excision of bilateral endometriomas. Am J Obstet Gynecol 2006;195:421-25.
87. Meuleman C, Tomassetti C, D’Hooghe TM. Clinical outcome after laparoscopic radical excision of endometriosis and laparoscopic segmental bowel resection. Curr Opin Obstet Gynecol 2012;24:245-52.
88. Meuleman C, Tomassetti C, D'Hoore A, et al. Surgical treatment of deeply infiltrating endometriosis with colorectal involvement. Hum Reprod Update 2011; 17:311-26.
89. De Cicco C, Corona R, Schonman R, Mailova K, Ussia A, Koninckx P. Bowel resection for deep endometriosis: a systematic review. BJOG 2011;118:285-91.
90. Martin DC. Hysterectomy for treatment of pain associated with endometriosis. JMinim Invasive Gynecol 2006;13:566-72.
91. Proctor ML, Latthe PM, Farquhar CM, Khan KS, Johnson NP. Surgical interruption of pelvic nerve pathways for primary and secondary dysmenorrhoea. Cochrane Database Syst Rev 2005;4:CD001896.
92. Hughes E, Brown J, Collins JJ, Farquhar C, Fedorkow DM, Vandekerckhove P. Ovulation suppression for endometriosis. Cochrane Database Syst Rev 2007;3:CD000155.
93. 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.
94. 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;21:2679-85.
95. Yap C, Furness S, Farquhar C. Pre and post operative medical therapy for endometriosis surgery. Cochrane Database Syst Rev 2004;3:CD003678.
96. Zegers-Hochschild F, Adamson GD, de Mouzon J, 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;92:1520-24.
97. Werbrouck E, Spiessens C, Meuleman C, D'Hooghe T. No difference in cycle pregnancy rate and in cumulative live-birth rate between women with surgically treated minimal to mild endometriosis and women with unexplained infertility after controlled ovarian hyperstimulation and intrauterine insemination. Fertil Steril 2006;86:566-71.
98. Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil Steril 2002;77:1148-55.
99. D'Hooghe TM, Denys B, Spiessens C, Meuleman C, Debrock S. Is the endometriosis recurrence rate increased after ovarian hyperstimulation? Fertil Steril 2006;86:283-90.
100. Coccia ME, Rizzello F, Gianfranco S. Does controlled ovarian hyperstimulation in women with a history of endometriosis influence recurrence rate? J Womens Health (Larchmt) 2010; 19: 2063-69.
101. Benaglia L, Somigliana E, Vercellini P, et al. The impact of IVF procedures on endometriosis recurrence. Eur J Obstet Gynecol Reprod Biol 2010;148:49-52.
102. Benaglia L, Pasin R, Somigliana E, Vercellini P, Ragni G, Fedele L. Unoperated ovarian endometriomas and responsiveness to hyperstimulation. Hum Reprod 2011;26:1356-61.
103. Sallam HN, Garcia-Velasco JA, Dias S, Arici A. Long-term pituitary down-regulation before in vitro fertilization (IVF) for women with endometriosis. Cochrane Database Syst Rev 2006;1:CD004635.
104. Opoien 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.
105. Vercellini P, Eskenazi B, Consonni D, et al. Oral contraceptives and risk of endometriosis: a systematic review and meta-analysis. Hum Reprod Update 2011;17:159-70.
106. Vitonis AF, Hankinson SE, Hornstein MD, Missmer SA. Adult physical activity and endometriosis risk. Epidemiology 2010;21:16-23.
107. Cramer DW, Wilson E, Stillman RJ, et al. The relation of endometriosis to menstrual characteristics, smoking, and exercise. JAMA 1986;255:1904-908.
108. Signorello LB1, Harlow BL, Cramer DW, Spiegelman D, Hill JA. Epidemiologic determinants of endometriosis: a hospital-based case-control study. Ann Epidemiol 1997;7:267-74.
109. Dhillon PK, Holt VL. Recreational physical activity and endometrioma risk. Am J Epidemiol 2003;158:156-64.
110. Heilier JF, Donnez J, Nackers F, et al. Environmental and host- associated risk factors in endometriosis and deep endometriotic nodules: a matched case-control study. Environ Res 2007;103:121-29.
111. Johnson NP, Hummelshoj L, World Endometriosis Society Montpellier Consortium. Consensus on current management of endometriosis. Hum Reprod 2013;28:1552-68.