European society of human reproduction and embryology guideline: management of women with endometriosis

Authors

  • G.A.J. Dunselman Research Institute GROW, Maastricht University Medical Centre, Maastricht, Netherlands
  • N. Vermeulen European Society of Human Reproduction and Embryology, Central Offi ce, Grimbergen, Belgium
  • C. Becker University of Oxford, John Radcliff e Hospital, Headington, Oxford, United Kingdom
  • C. Calhaz-Jorge CHLN/Hospital de Santa Maria, Lisboa, Portugal
  • T. D’hooghe Department of Obstetrics and Gynecology, Department of Development and Regeneration, Leuven, Belgium
  • B. De Bie Endometriose Stichting, Sittard-Geleen, Netherlands
  • O. Heikinheimo Kaёtiloёopisto hospital, Finland
  • A.W. Horne MRC Centre for Reproductive Health, University of Edinburgh, Edinburgh, United Kingdom
  • L. Kiesel University Hospital of Muёnster, Muёnster/Westf, Germany
  • A. Nap Rijnstate Arnhem, Arnhem, Netherlands
  • A. Prentice The Rosie Hospital, Cambridge, United Kingdom
  • E. Saridogan University College London Hospital, Women’s Health Division, London, United Kingdom
  • D. Soriano Endometriosis Center, Sheba Medical Center, Ramat Gan, Israel
  • W. Nelen Radboud University Nijmegen Medical Centre, Nijmegen, Netherlands

DOI:

https://doi.org/10.18370/2309-4117.2014.19.54-67

Keywords:

endometriosis, European Society of Human Reproduction and Embryology, guideline, evidence based

Abstract

Study question: What is the optimal management of women with endometriosis based on the best available evidence in the literature?

Summary answer: Using the structured methodology of the Manual for ESHRE Guideline Development, 83 recommendations were formulated that answered the 22 key questions on optimal management of women with endometriosis.

What is known already: The European Society of Human Reproduction and Embryology (ESHRE) guideline for the diagnosis and treatment of endometriosis (2005) has been a reference point for best clinical care in endometriosis for years, but this guideline was in need of updating.

Study design, size, duration: This guideline was produced by a group of experts in the field using the methodology of the Manual for ESHRE Guideline Development, including a thorough systematic search of the literature, quality assessment of the included papers up to January 2012 and consensus within the guideline group on all recommendations.

Main results and the role of chance: The guideline provides 83 recommendations on diagnosis of endometriosis and on the treatment of endometriosis-associated pain and infertility, on the management of women in whom the disease is found incidentally (without pain or infertility), on prevention of recurrence of disease and/or painful symptoms, on treatment of menopausal symptoms in patients with a history of endometriosis and on the possible association of endometriosis and malignancy.

Limitations: We identified several areas in care of women with endometriosis for which robust evidence is lacking. These areas were addressed by formulating good practice points (GPP), based on the expert opinion of the guideline group members.

Wider implications of the findings: Since 32 out of the 83 recommendations for the management of women with endometriosis could not be based on high level evidence and therefore were GPP, the guideline group formulated research recommendations to guide future research with the aim of increasing the body of evidence.

Study funding/competing interest(s): The guideline was developed and funded by ESHRE, covering expenses associated with the guideline meetings, with the literature searches and with the implementation of the guideline. The guideline group members did not receive payment. All guideline group members disclosed any relevant conflicts of interest.

Author Biographies

G.A.J. Dunselman, Research Institute GROW, Maastricht University Medical Centre, Maastricht

Department of Obstetrics&Gynaecology

C. Becker, University of Oxford, John Radcliff e Hospital, Headington, Oxford

Nuffi eld Department of Obstetrics and Gynaecology

C. Calhaz-Jorge, CHLN/Hospital de Santa Maria, Lisboa

Faculdade de Medicina da Universidade de Lisboa, Human Reproduction Unit, Department of Obstetrics and Gynecology

T. D’hooghe, Department of Obstetrics and Gynecology, Department of Development and Regeneration, Leuven

Отделение акушерства и гинекологии

O. Heikinheimo, Kaёtiloёopisto hospital

Department of Obstetrics and Gynecology

A.W. Horne, MRC Centre for Reproductive Health, University of Edinburgh, Edinburgh

Центр репродуктивного здоровья MRC

A. Prentice, The Rosie Hospital, Cambridge

Department of Obstetrics and Gynaecology

References

  1. Abou-Setta AM., Al-Inany H.G., Farquhar C.M. «Levonorgestrel-releasing intrauterine device (LNG-IUD) for symptomatic endometriosis following surgery.» Cochrane Database Syst Rev (2006):CD005072.
  2. Agarwal A., Gupta S., Sharma R.K. «Role of oxidative stress in female reproduction.» Reprod Biol Endocrinol, 3(2005):28.
  3. Ahmad G., Duff y J.M., Farquhar C., Vail A., Vandekerckhove P., Watson A., Wiseman D. «Barrier agents for adhesion prevention after gynaecological surgery.» Cochrane Database Syst Rev (2008):CD000475.
  4. Al Kadri H., Hassan S., Al-Fozan H.M., Hajeer A. «Hormone therapy for endometriosis and surgical menopause.» Cochrane Database Syst Rev (2009):CD005997.
  5. Allen C., Hopewell S., Prentice A., Gregory D. «Nonsteroidal anti-infl ammatory drugs for pain in women with endometriosis.» Cochrane Database Syst Rev (2009):CD004753.
  6. Astin J.A., Marie A., Pelletier K.R., Hansen E., Haskell W.L. «A review of the incorporation of complementary and alternative medicine by mainstream physicians.» Arch Intern Med, 158(1998):2303-2310.
  7. Ballard K., Lowton K., Wright J. «What’s the delay? A qualitative study of women’s experiences of reaching a diagnosis of endometriosis.» Fertil Steril, 86(2006):1296-1301.
  8. Ballard K.D., Seaman H.E., de Vries C.S., Wright J.T. «Can symptomatology help in the diagnosis of endometriosis?» Findings from a national case-control study–Part 1. BJOG, 115(2008):1382-1391.
  9. Barnhart K., Dunsmoor-Su R., Coutifaris C. «Eff ect of endometriosis on in vitro fertilization.» Fertil Steril, 77(2002):1148-1155.
  10. Bazot M., Lafont C., Rouzier R., Roseau G., Thomassin-Naggara I., Darai E. «Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis.» Fertil Steril, 92(2009):1825-1833.
  11. Bellelis P., Dias J.A. Jr., Podgaec S., Gonzales M., Baracat E.C., Abrao M.S. «Epidemiological and clinical aspects of pelvic endometriosis-a case series.» Rev Assoc Med Bras, 56(2010):467-471.
  12. Benaglia L., Somigliana E., Iemmello R., Colpi E., Nicolosi A.E., Ragni G. «Endometrioma and oocyte retrieval-induced pelvic abscess: a clinical concern or an exceptional complication?.» Fertil Steril, 89(2008):1263-1266.
  13. Benaglia L., Somigliana E., Vercellini P., Benedetti F., Iemmello R., Vighi V., Santi G., Ragni G. «The impact of IVF procedures on endometriosis recurrence.» Eur J Obstet Gynecol Reprod Biol, 148(2010):49-52.
  14. Benaglia L., Somigliana E., Santi G., Scarduelli C., Ragni G., Fedele L. «IVF and endometriosis-related symptom progression: insights from a prospective study.» Hum Reprod, 26(2011):2368-2372.
  15. Benschop L., Farquhar C., van der Poel N., Heineman M.J. «Interventions for women with endometrioma prior to assisted reproductive technology.» Cochrane Database Syst Rev (2010):CD008571.
  16. Bergqvist A. «Extragenital endometriosis.» Areview. Eur J Surg, 158(1992):7-12.
  17. Bergqvist A., Jacobson J., Harris S. «A double-blind randomized study of the treatment of endometriosis with nafarelin or nafarelin plus norethisterone.» Gynecol Endocrinol, 11(1997):187-194.
  18. Bianchi P.H., Pereira R.M., Zanatta A., Alegretti J.R., Motta E.L., Serafi ni P.C. «Extensive excision of deep infi ltrative endometriosis before in vitro fertilization signifi cantly improves pregnancy rates.» J Minim Invasive Gynecol, 16(2009): 174-180.
  19. Brown C.B., Luciano A.A., Martin D., Peers E., Scrimgeour A., di Zerega G.S. «Adept Adhesion Reduction Study G. Adept (icodextrin 4% solution) reduces adhesions after laparoscopic surgery for adhesiolysis: a double-blind, randomized, controlled study.» Fertil Steril, 88(2007):1413-1426.
  20. Brown J., Pan A., Hart R.J. «Gonadotrophin-releasing hormone analogues for pain associated with endometriosis.» Cochrane Database Syst Rev (2010):CD008475.
  21. Brown J., Kives S., Akhtar M. «Progestagens and anti-progestagens for pain associated with endometriosis.» Cochrane Database Syst Rev, 3(2012):CD002122.
  22. Burks-Wicks C., Cohen M., Fallbacher J., RNT, Wieser F. «А Western primer of Chinese herbal therapy in endometriosis and infertility.» Womens Health (Lond Engl),1(2005):447-463.
  23. Carmona F., Martinez-Zamora M.A., Rabanal A., Martinez-Roman S., Balasch J. «Ovarian cystectomy versus laser vaporization in the treatment of ovarian endometriomas: a randomized clinical trial with a fi ve-year follow-up.» Fertil Steril, 96(2011):251-254.
  24. Chan E. «Quality of effi cacy research in complementary and alternative medicine.» JAMA, 299(2008):2685-2686.
  25. Chang F.H., Chou H.H., Soong Y.K., Chang M.Y., Lee C.L., Lai Y.M. «Effi cacy of isotopic 13CO2 laser laparoscopic evaporation in the treatment of infertile patients with minimal and mild endometriosis: a life table cumulative pregnancy rates study.» J Am Assoc Gynecol Laparosc, 4(1997):219-223.
  26. Chapron C., Dubuisson J.B., Pansini V., Vieira M., Fauconnier A., Barakat H., Dousset B. «Routine clinical examination is not suffi cient for diagnosing and locating deeply infi ltrating endometriosis.» J Am Assoc Gynecol Laparosc, 9(2002):115-119.
  27. Chapron C., Souza C., Borghese B., Lafay-Pillet M.C., Santulli P., Bijaoui G., Goffi net .F, de Ziegler D. «Oral contraceptives and endometriosis: the past use of oral contraceptives for treating severe primary dysmenorrhea is associated with endometriosis, especially deep infi ltrating endometriosis.» Hum Reprod, 26(2011):2028-2035.
  28. Coccia M.E., Rizzello F., Gianfranco S. «Does controlled ovarian hyperstimulation in women with a history of endometriosis infl uence recurrence rate?» J Womens Health (Larchmt), 19(2010):2063-2069.
  29. Condous G., Van Calster B., Van Huff el S., Lam A. «What is the value of preoperative bimanual pelvic examination in women undergoing laparoscopic total hysterectomy?» J MinimInvasive Gynecol, 14(2007):334-338.
  30. D’Hooghe T.M., Denys B., Spiessens C., Meuleman C., Debrock S. «Is the endometriosis recurrence rate increased after ovarian hyperstimulation?» Fertil Steril, 86(2006):283-290.
  31. Davis G.D., Thillet E., Lindemann J. «Clinical characteristics of adolescent endometriosis.» J Adolesc Health, 14(1993):362-368.
  32. Davis L., Kennedy S.S., Moore J., Prentice A. «Modern combined oral contraceptives for pain associated with endometriosis.» Cochrane Database Syst Rev (2007):CD001019.
  33. De Cicco C., Corona R., Schonman R., Mailova K., Ussia A., Koninckx P. «Bowel resection for deep endometriosis: a systematic review.» BJOG, 118(2011):285-291.
  34. Donnez J., Squiffl et 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, 25(2010):1949-1958.
  35. Donnez J., Wyns C., Nisolle M. «Does ovarian surgery for endometriomas impair the ovarian response to gonadotropin?» Fertil Steril, 76(2001):662-665.
  36. Eisenberg D.M., Davis R.B., Ettner S.L., Appel S., Wilkey S., Van Rompay M.,
  37. Kessler R.C. «Trends in alternative medicine use in the United States, 1990–1997: results of a follow-up national survey.» JAMA, 280(1998):1569-1575.
  38. Eskenazi B., Warner M.L. «Epidemiology of endometriosis.» Obstet Gynecol Clin North Am, 24(1997):235-258.
  39. Eskenazi B., Warner M., Bonsignore L., Olive D., Samuels S., Vercellini P. «Validation study of nonsurgical diagnosis of endometriosis.» Fertil Steril, 76(2001):929-935.
  40. Ferreira R.A., Vieira C.S., Rosa E.S.J.C., Rosa-e-Silva A.C., Nogueira A.A., Ferriani R.A. «Eff ects of the levonorgestrel-releasing intrauterine system on cardiovascular risk markers in patients with endometriosis: a comparative study with the GnRH analogue.» Contraception, 81(2010):117-122.
  41. Ferrero S., Gillott D.J., Venturini P.L., Remorgida V. «Use of aromatase inhibitors to treat endometriosis-related pain symptoms: a systematic review.» Reprod Biol Endocrinol, 9(2011):89.
  42. Flower A., Liu J.P., Chen S., Lewith G., Little P. «Chinese herbal medicine for endometriosis.» Cochrane Database Syst Rev (2009):CD006568.
  43. Forman R.G., Robinson J.N., Mehta Z., Barlow D.H. «Patient history as a simple predictor of pelvic pathology in subfertile women.» Hum Reprod, 8(1993):53-55.
  44. Furness S., Yap C., Farquhar C., Cheong Y. «Pre and post-operative medical therapy for endometriosis surgery.» Cochrane Database Syst Rev (2004):CD003678.
  45. Gerhard I., Postneek F. «Auricular acupuncture in the treatment of female infertility.» Gynecol Endocrinol, 6(1992):171-181.
  46. Gomes M.K., Ferriani R.A., Rosa e Silva J.C., Japur de Sa Rosa e Silva A.C., Vieira C.S., Candido dos Reis F.J. «The levonorgestrel-releasing intrauterine system and endometriosis staging.» Fertil Steril, 87(2007):1231-1234.
  47. Gylfason J.T., Kristjansson K.A., Sverrisdottir G., Jonsdottir K., Rafnsson V., Geirsson R.T. «Pelvic endometriosis diagnosed in an entire nation over 20 years.» Am J Epidemiol, 172(2010):237-243.
  48. Harris P., Rees R. «The prevalence of complementary and alternative medicine use among the general population: a systematic review of the literature.» Complement Ther Med, 8(2000):88-96.
  49. Hart R.J., Hickey M., Maouris P., Buckett W. «Excisional surgery versus ablative surgery for ovarian endometriomata.» Cochrane Database Syst Rev (2008):CD004992.
  50. Healey M., Ang W.C., Cheng C. «Surgical treatment of endometriosis: a prospective randomized double-blinded trial comparing excision and ablation.» Fertil Steril, 94(2010):2536-2540.
  51. Hudelist G., English J., Thomas A.E., Tinelli A., Singer C.F., Keckstein J. «Diagnostic accuracy of transvaginal ultrasound for non-invasive diagnosis of bowel endometriosis: systematic review and meta-analysis.» Ultrasound Obstet Gynecol, 37(2011):257-263.
  52. Hudelist G., Fritzer N., Thomas A., Niehues C., Oppelt P., Haas D., Tammaa A., Salzer H. «Diagnostic delay for endometriosis in Austria and Germany: causes and possible consequences.» Hum Reprod, 27(2012):3412-3416.
  53. Hughes E., Brown J., Collins J.J., Farquhar C., Fedorkow D.M., Vandekerckhove P. «Ovulation suppression for endometriosis.» Cochrane Database Syst Rev (2007):CD000155.
  54. Jacobson T.Z., Duff y J.M., Barlow D., Koninckx P.R., Garry R. «Laparoscopic surgery for pelvic pain associated with endometriosis.» Cochrane Database Syst Rev (2009):CD001300.
  55. Jacobson T.Z., Duff y J.M., Barlow D., Farquhar C., Koninckx P.R., Olive D. «Laparoscopic surgery for subfertility associated with endometriosis.» Cochrane Database Syst Rev (2010):CD001398.
  56. Jenkins T.R., Liu C.Y., White J. «Does response to hormonal therapy predict presence or absence of endometriosis?» J Minim Invasive Gynecol 15(2008):82-86.
  57. Joseph J., Sahn S.A. «Thoracic endometriosis syndrome: newobservations from an analysis of 110 cases.» Am J Med, 100(1996):164-170.
  58. Jubanyik K.J., Comite F. «Extrapelvic endometriosis.» Obstet Gynecol Clin North Am, 24(1997):411-440.
  59. Kennedy S., Bergqvist A., Chapron C., D’Hooghe T., Dunselman G., Greb R., Hummelshoj L., Prentice A., Saridogan E. «ESHRE Special Interest Group for Endometriosis and Endometrium Guideline Development. ESHRE guideline for the diagnosis and treatment of endometriosis.» Hum Reprod, 20(2005):2698-2704.
  60. Kondo W., Bourdel N., Tamburro S., Cavoli D., Jardon K., Rabischong B., Botchorishvili R., Pouly J., Mage G., Canis M. «Complications after surgery for deeply infi ltrating pelvic endometriosis.» BJOG, 118(2011):292-298.
  61. Koninckx P.R., Meuleman C., Oosterlynck D., Cornillie F.J. «Diagnosis of deep endometriosis by clinical examination during menstruation and plasma CA-125 concentration.» Fertil Steril, 65(1996):280-287.
  62. Lemaire G.S. «More than just menstrual cramps: symptoms and uncertainty among women with endometriosis.» J Obstet Gynecol Neonatal Nurs, 33(2004):71-79.
  63. Liang C.C., Tsai C.C., Chen T.C., Soong Y.K. «Management of perineal endometriosis.» Int J Gynaecol Obstet, 53(1996):261-265.
  64. Ling F.W. «Randomized controlled trial of depot leuprolide in patients with chronic pelvic pain and clinically suspected endometriosis.» Pelvic Pain Study Group. Obstet Gynecol, 93(1999):51-58.
  65. Luscombe G.M., Markham R., Judio M., Grigoriu A., Fraser I.S. «Abdominal bloating: an under-recognized endometriosis symptom.» J Obstet Gynaecol Can, 31(2009):1159-1171.
  66. Makarainen L., Ronnberg L., Kauppila A. «Medroxyprogesterone acetate supplementation diminishes the hypoestrogenic side eff ects of gonadotropin-releasing hormone agonist without changing its effi cacy in endometriosis.» Fertil Steril, 65(1996):29-34.
  67. Marinis A., Vassiliou J., Kannas D., Theodosopoulos T.K., Kondi-Pafi ti A., Kairi E., Smyrniotis V. «Endometriosis mimicking soft tissue tumors: diagnosis and treatment.» Eur J Gynaecol Oncol, 27(2006):168-170.
  68. Marjoribanks J., Proctor M., Farquhar C., Derks R.S. «Nonsteroidal anti-infl ammatory drugs for dysmenorrhoea.» Cochrane Database Syst Rev (2010):CD001751.
  69. May K.E., Conduit-Hulbert S.A., Villar J., Kirtley S., Kennedy S.H., Becker C.M. «Peripheral biomarkers of endometriosis: a systematic review.» Hum Reprod Update, 16(2010):651-674.
  70. May K.E., Villar J., Kirtley S., Kennedy S.H., Becker C.M. «Endometrial alterations in endometriosis: a systematic review of putative biomarkers.» Hum Reprod Update, 17(2011):637-653.
  71. Meuleman C., Vandenabeele B., Fieuws S., Spiessens C., Timmerman D., D’Hooghe T. «High prevalence of endometriosis in infertile women with normal ovulation and normospermic partners.» Fertil Steril, 92(2009):68-74.
  72. Meuleman C., D’Hoore A., Van Cleynenbreugel B., Tomassetti C., D’Hooghe T. «Why we need international agreement on terms and defi nitions to assess clinical outcome after endometriosis surgery.» Hum Reprod, 26(2011a):1598-1599; author reply 1599-1600.
  73. Meuleman C.,Tomassetti C., D’Hoore A., Van Cleynenbreugel B., Penninckx F., Vergote I., D’Hooghe T. «Surgical treatment of deeply infi ltrating endometriosis with colorectal involvement.» Hum Reprod Update, 17(2011b):311-326.
  74. Moen M.H., Stokstad T. «A long-term follow-up study of women with asymptomatic endometriosis diagnosed incidentally at sterilization.» Fertil Steril, 78(2002):773-776.
  75. Moghissi K.S., Schlaff W.D., Olive D.L., Skinner M.A., Yin H. «Goserelin acetate (Zoladex) with or without hormone replacement therapy for the treatment of endometriosis.» Fertil Steril, 69(1998):1056-1062.
  76. Mol B.W., Bayram N., Lijmer J.G.,Wiegerinck M.A., Bongers M.Y., van der Veen F., Bossuyt P.M. «The performance of CA-125 measurement in the detection of endometriosis: a meta-analysis.» Fertil Steril, 70(1998):1101-1108.
  77. 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, 20(2002):630-634.
  78. Nawathe A., Patwardhan S., Yates D., Harrison G.R., Khan K.S. «Systematic review of the eff ects of aromatase inhibitors on pain associated with endometriosis.» BJOG, 115(2008):818-822.
  79. Nezhat C., Crowgey S., Nezhat F. «Videolaseroscopy for the treatment of endometriosis associated with infertility.» Fertil Steril, 51(1989):237-240.
  80. Nezhat C., Hajhosseini B., King L.P. «Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis.» JSLS, 15(2011):387-392.
  81. Nisolle M., Pasleau F., Foidart J.M. «Extragenital endometriosis.» J Gynecol Obstet Biol Reprod (Paris), 36(2007):173-178.
  82. Nissotakis C., Zouros E., Revelos K., Sakorafas G.H. «Abdominal wall endometrioma: a case report and review of the literature.» AORN J, 91(2010):730-742; quiz 743-735.
  83. Nnoaham K.E., Hummelshoj L., Webster P., d’Hooghe T., de Cicco Nardone F., de Cicco Nardone C., Jenkinson C., Kennedy S.H., Zondervan K.T. «World Endometriosis Research Foundation Global Study of Women’s Health consortium. Impact of endometriosis on quality of life and work productivity: a multicenter study across ten countries.» Fertil Steril, 96(2011):366-373 e368.
  84. Nowroozi K., Chase J.S., Check J.H., Wu C.H. «The importance of laparoscopic coagulation of mild endometriosis in infertile women.» Int J Fertil, 32(1987):442-444.
  85. Nulsen J.C., Walsh S., Dumez S., Metzger D.A. «A randomized and longitudinal study of human menopausal gonadotropin with intrauterine insemination in the treatment of infertility.» Obstet Gynecol, 82(1993):780-786.
  86. Olive D.L., Stohs G.F., Metzger D.A., Franklin R.R. «Expectant management and hydrotubations in the treatment of endometriosisassociated infertility.» Fertil Steril, 44(1985):35-41.
  87. Opoien H.K., Fedorcsak P., Byholm T., Tanbo T. «Complete surgical removal of minimal and mild endometriosis improves outcome of subsequent IVF/ICSI treatment.» Reprod Biomed Online, 23(2011):389-395.
  88. 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, 88(2007):832-839.
  89. Papaleo E., Ottolina J., Vigano P., Brigante C., Marsiglio E., De Michele F., Candiani M. «Deep pelvic endometriosis negatively aff ects ovarian reserve and the number of oocytes retrieved for in vitro fertilization.» Acta Obstet Gynecol Scand, 90(2011):878-884.
  90. Pascual M.A., Guerriero S., Hereter L., Barri-Soldevila P., Ajossa S., Graupera B., Rodriguez I. «Diagnosis of endometriosis of the rectovaginal septum using introital threedimensional ultrasonography.» Fertil Steril, 94(2010):2761-2765.
  91. Petta C.A., Ferriani R.A., Abrao M.S., Hassan D., Rosa E.S.J.C., Podgaec S., Bahamondes L. «Randomized clinical trial of a levonorgestrel-releasing intrauterine system and a depot GnRH analogue for the treatment of chronic pelvic pain in women with endometriosis.» Hum Reprod, 20(2005):1993-1998.
  92. Proctor M.L., Smith C.A., Farquhar C.M., Stones R.W. «Transcutaneous electrical nerve stimulation and acupuncture for primary dysmenorrhoea.» Cochrane Database Syst Rev (2002):CD002123.
  93. Proctor M., Latthe P., Farquhar C., Khan K., Johnson N. «Surgical interruption of pelvic nerve pathways for primary and secondary dysmenorrhoea.» Cochrane Database Syst Rev (2005):CD001896.
  94. Jenkins T.R., Liu C.Y., White J. «Does response to hormonal therapy predict presence or absence of endometriosis?» J Minim Invasive Gynecol, 15(2008):82-86.
  95. Joseph J., Sahn S.A. «Thoracic endometriosis syndrome: newobservations from an analysis of 110 cases.» Am J Med, 100(1996):164-170.
  96. Jubanyik K.J., Comite F. «Extrapelvic endometriosis.» Obstet Gynecol Clin North Am, 24(1997):411-440.
  97. Kennedy S., Bergqvist A., Chapron C., D’Hooghe T., Dunselman G., Greb R., Hummelshoj L., Prentice A., Saridogan E. «ESHRE Special Interest Group for Endometriosis and Endometrium Guideline Development. ESHRE guideline for the diagnosis and treatment of endometriosis.» Hum Reprod, 20(2005):2698-2704.
  98. Kondo W., Bourdel N., Tamburro S., Cavoli D., Jardon K., Rabischong B., Botchorishvili R., Pouly J., Mage G., Canis M. «Complications after surgery for deeply infi ltrating pelvic endometriosis.» BJOG, 118(2011):292-298.
  99. Koninckx P.R., Meuleman C., Oosterlynck D., Cornillie F.J. «Diagnosis of deep endometriosis by clinical examination during menstruation and plasma CA-125 concentration.» Fertil Steril, 65(1996):280-287.
  100. Lemaire G.S. «More than just menstrual cramps: symptoms and uncertainty among women with endometriosis.» J Obstet Gynecol Neonatal Nurs, 33(2004):71-79.
  101. Liang C.C., Tsai C.C., Chen T.C., Soong Y.K. «Management of perineal endometriosis.» Int J Gynaecol Obstet, 53(1996):261-265.
  102. Ling F.W. «Randomized controlled trial of depot leuprolide in patients with chronic pelvic pain and clinically suspected endometriosis.» Pelvic Pain Study Group. Obstet Gynecol, 93(1999):51-58.
  103. Luscombe G.M., Markham R., Judio M., Grigoriu A., Fraser I.S. «Abdominal bloating: an under-recognized endometriosis symptom.» J Obstet Gynaecol Can, 31(2009):1159-1171.
  104. Makarainen L., Ronnberg L., Kauppila A. «Medroxyprogesterone acetate supplementation diminishes the hypoestrogenic side eff ects of gonadotropin-releasing hormone agonist without changing its effi cacy in endometriosis.» Fertil Steril, 65(1996):29-34.
  105. Marinis A., Vassiliou J., Kannas D., Theodosopoulos T.K., Kondi-Pafi ti A., Kairi E., Smyrniotis V. «Endometriosis mimicking soft tissue tumors: diagnosis and treatment.» Eur J Gynaecol Oncol, 27(2006):168-170.
  106. Marjoribanks J., Proctor M., Farquhar C., Derks R.S. «Nonsteroidal anti-infl ammatory drugs for dysmenorrhoea.» Cochrane Database Syst Rev (2010):CD001751.
  107. May K.E., Conduit-Hulbert S.A., Villar J., Kirtley S., Kennedy S.H., Becker C.M. «Peripheral biomarkers of endometriosis: a systematic review.» Hum Reprod Update, 16(2010):651-674.
  108. May K.E., Villar J., Kirtley S., Kennedy S.H., Becker C.M. «Endometrial alterations in endometriosis: a systematic review of putative biomarkers.» Hum Reprod Update, 17(2011):637-653.
  109. Meuleman C., Vandenabeele B., Fieuws S., Spiessens C., Timmerman D., D’Hooghe T. «High prevalence of endometriosis in infertile women with normal ovulation and normospermic partners.» Fertil Steril, 92(2009):68-74.
  110. Meuleman C., D’Hoore A., Van Cleynenbreugel B., Tomassetti C., D’Hooghe T. «Why we need international agreement on terms and defi nitions to assess clinical outcome after endometriosis surgery.» Hum Reprod, 26(2011a):1598-1599; author reply 1599-1600.
  111. Meuleman C., Tomassetti C., D’Hoore A., Van Cleynenbreugel B., Penninckx F., Vergote I., D’Hooghe T. «Surgical treatment of deeply infi ltrating endometriosis with colorectal involvement.» Hum Reprod Update, 17(2011b):311-326.
  112. Moen M.H., Stokstad T. «A long-term follow-up study of women with asymptomatic endometriosis diagnosed incidentally at sterilization.» Fertil Steril, 78(2002):773-776.
  113. Moghissi K.S., Schlaff W.D., Olive D.L., Skinner M.A., Yin H. «Goserelin acetate (Zoladex) with or without hormone replacement therapy for the treatment of endometriosis.» Fertil Steril, 69(1998):1056-1062.
  114. Mol B.W., Bayram N., Lijmer J.G., Wiegerinck M.A., Bongers M.Y., van der Veen F., Bossuyt P.M. «The performance of CA-125 measurement in the detection of endometriosis: a meta-analysis.» Fertil Steril, 70(1998):1101-1108.
  115. 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, 20(2002):630-634.
  116. Nawathe A., Patwardhan S., Yates D., Harrison G.R., Khan K.S. «Systematic review of the eff ects of aromatase inhibitors on pain associated with endometriosis.» BJOG, 115(2008):818-822.
  117. Nezhat C., Crowgey S., Nezhat F. «Videolaseroscopy for the treatment of endometriosis associated with infertility.» Fertil Steril, 1989;51:237–240.
  118. Nezhat C., Hajhosseini B., King L.P. «Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis.» JSLS, 15(2011):387-392.
  119. Nisolle M., Pasleau F., Foidart J.M. «Extragenital endometriosis.» J Gynecol Obstet Biol Reprod (Paris), 36(2007):173-178.
  120. Nissotakis C., Zouros E., Revelos K., Sakorafas G.H. «Abdominal wall endometrioma: a case report and review of the literature.» AORN J, 91(2010):730-742; quiz 743-735.
  121. Nnoaham K.E., Hummelshoj L., Webster P., d’Hooghe T., de Cicco Nardone F., de Cicco Nardone C., Jenkinson C., Kennedy S.H., Zondervan K.T. «World Endometriosis Research Foundation Global Study of Women’s Health consortium.» Impact of endometriosis on quality of life and work productivity: a multicenter study across ten countries. Fertil Steril, 96(2011):366-373 e368.
  122. Nowroozi K., Chase J.S., Check J.H., Wu C.H. «The importance of laparoscopic coagulation of mild endometriosis in infertile women.» Int J Fertil, 32(1987):442-444.
  123. Nulsen J.C., Walsh S., Dumez S., Metzger D.A. «A randomized and longitudinal study of human menopausal gonadotropin with intrauterine insemination in the treatment of infertility.» Obstet Gynecol, 82(1993):780-786.
  124. Olive D.L., Stohs G.F., Metzger D.A., Franklin R.R. «Expectant management and hydrotubations in the treatment of endometriosisassociated infertility.» Fertil Steril, 44(1985):35-41.
  125. Opoien H.K., Fedorcsak P., Byholm T., Tanbo T. «Complete surgical removal of minimal and mild endometriosis improves outcome of subsequent IVF/ICSI treatment.» Reprod Biomed Online, 23(2011):389-395.
  126. 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, 88(2007):832-839.
  127. Papaleo E., Ottolina J., Vigano P., Brigante C., Marsiglio E., De Michele F., Candiani M. «Deep pelvic endometriosis negatively aff ects ovarian reserve and the number of oocytes retrieved for in vitro fertilization.» Acta Obstet Gynecol Scand, 90(2011):878-884.
  128. Pascual M.A., Guerriero S., Hereter L., Barri-Soldevila P., Ajossa S., Graupera B., Rodriguez I. «Diagnosis of endometriosis of the rectovaginal septum using introital threedimensional ultrasonography.» Fertil Steril, 94(2010):2761-2765.
  129. Petta C.A., Ferriani R.A., Abrao M.S., Hassan D., Rosa E.S.J.C., Podgaec S., Bahamondes L. «Randomized clinical trial of a levonorgestrel-releasing intrauterine system and a depot GnRH analogue for the treatment of chronic pelvic pain in women with endometriosis.» Hum Reprod, 20(2005):1993-1998.
  130. Proctor M.L., Smith C.A., Farquhar C.M., Stones R.W. «Transcutaneous electrical nerve stimulation and acupuncture for primary dysmenorrhoea.» Cochrane Database Syst Rev (2002):CD002123.
  131. Proctor M., Latthe P., Farquhar C., Khan K., Johnson N. «Surgical interruption of pelvic nerve pathways for primary and secondary dysmenorrhoea.» Cochrane Database Syst Rev (2005):CD001896.
  132. Rawson J.M. «Prevalence of endometriosis in asymptomatic women.» J Reprod Med, 36(1991):513-515.
  133. Ripps B.A., Martin D.C. «Correlation of focal pelvic tenderness with implant dimension and stage of endometriosis.» J Reprod Med, 37(1992):620-624.
  134. Sallam H.N., Garcia-Velasco J.A., Dias S., Arici A. «Long-term pituitary down-regulation before in vitro fertilization (IVF) for women with endometriosis.» Cochrane Database Syst Rev (2006):CD004635.
  135. Scottish Intercollegiate Guidelines Network EH, 8-10 Hillside Crescent, Edinburgh EH7 5EA. 2010. www.sign.ac.uk (12 December 2013, date last accessed).
  136. Seracchioli R., Mabrouk M., Guerrini M., Manuzzi L., Savelli L., Frasca C., Venturoli S. «Dyschezia and posterior deep infi ltrating endometriosis: analysis of 360 cases.» J Minim Invasive Gynecol, 15(2008):695-699.
  137. Seracchioli R., Mabrouk M., Manuzzi L., Vicenzi C., Frasca C., Elmakky A., Venturoli S. «Post-operative use of oral contraceptive pills for prevention of anatomical relapse or symptom-recurrence after conservative surgery for endometriosis.» Hum Reprod, 24(2009):2729-2735.
  138. Sesti F., Pietropolli A., Capozzolo T., Broccoli P., Pierangeli S., Bollea M.R., Piccione E. «Hormonal suppression treatment or dietary therapy versus placebo in the control of painful symptoms after conservative surgery for endometriosis stage III–IV.» A randomized comparative trial. Fertil Steril, 88(2007):1541-1547.
  139. Song J.Y., Borncamp E., Mehaff ey P., Rotman C. «Large abdominal wall endometrioma following laparoscopic hysterectomy.» JSLS, 15(2011):261-263.
  140. Stratton P., Winkel C., Premkumar A., Chow C., Wilson J., Hearns-Stokes R., Heo S., Merino M., Nieman L.K. «Diagnostic accuracy of laparoscopy, magnetic resonance imaging, and histopathologic examination for the detection of endometriosis.» Fertil Steril, 79(2003):1078-1085.
  141. Taskin O., Yalcinoglu A.I., Kucuk S., Uryan I., Buhur A., Burak F. «Eff ectiveness of tibolone on hypoestrogenic symptoms induced by goserelin treatment in patients with endometriosis.» Fertil Steril, 67(1997):40-45.
  142. Thomassin I., Bazot M., Detchev R., Barranger E., Cortez A., Darai E. «Symptoms before and after surgical removal of colorectal endometriosis that are assessed by magnetic resonance imaging and rectal endoscopic sonography.» Am J Obstet Gynecol, 190(2004):1264-1271.
  143. Trew G., Pistofi dis G., Pados G., Lower A., Mettler L., Wallwiener D., Korell M., Pouly J.L., Coccia M.E., Audebert A. et al. «Gynaecological endoscopic evaluation of 4% icodextrin solution: a European, multicentre, double-blind, randomized study of the effi cacy and safety in the reduction of de novo adhesions after laparoscopic gynaecological surgery.» Hum Reprod, 26(2011):2015-2027.
  144. Tummon I.S., Asher L.J., Martin J.S., Tulandi T. «Randomized controlled trial of superovulation and insemination for infertility associated with minimal or mild endometriosis.» Fertil Steril, 68(1997):8-12.
  145. Van Holsbeke C., Van Calster B., Guerriero S., Savelli L., Paladini D., Lissoni A.A., Czekierdowski A., Fischerova D., Zhang J., Mestdagh G. et al. «Endometriomas: their ultrasound characteristics.» Ultrasound Obstet Gynecol, 35(2010):730-740.
  146. Vercellini P., Trespidi L., Colombo A., Vendola N., Marchini M., Crosignani P.G. «A gonadotropin-releasing hormone agonist versus a low-dose oral contraceptive for pelvic pain associated with endometriosis.» Fertil Steril, 60(1993):75-79.
  147. Vercellini P., Frontino G., De Giorgi O., Pietropaolo G., Pasin R., Crosignani P.G. «Continuous use of an oral contraceptive for endometriosis-associated recurrent dysmenorrhea that does not respond to a cyclic pill regimen» Fertil Steril, 80(2003):560-563.
  148. Vercellini P., Fedele L., Aimi G., De Giorgi O., Consonni D., Crosignani P.G. «Reproductive performance, pain recurrence and disease relapse after conservative surgical treatment for endometriosis: the predictive value of the current classifi cation system.» Hum Reprod, 21(2006):2679-2685.
  149. Vercellini P., Barbara G., Somigliana E., Bianchi S., Abbiati A., Fedele L. «Comparison of contraceptive ring and patch for the treatment of symptomatic endometriosis.» Fertil Steril, 93(2010a):2150-2161.
  150. Vercellini P., Somigliana E., Vigano P., De Matteis S., Barbara G., Fedele L. «Post-operative endometriosis recurrence: a plea for prevention based on pathogenetic, epidemiological and clinical evidence.» Reprod Biomed Online, 21(2010b):259-265.
  151. Vercellini P., Eskenazi B., Consonni D., Somigliana E., Parazzini F., Abbiati A., Fedele L. «Oral contraceptives and risk of endometriosis: a systematic review and metaanalysis.» Hum Reprod Update, 17(2011):159-170.
  152. Vitonis A.F., Hankinson S.E., Hornstein M.D., Missmer S.A. «Adult physical activity and endometriosis risk.» Epidemiology, 21(2010):16-23.
  153. Werbrouck E., Spiessens C., Meuleman C., D’HoogheT. «Nodiff erence 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, 86(2006):566-571.
  154. Wright J., Lotfallah H., Jones K., Lovell D. «A randomized trial of excision versus ablation for mild endometriosis.» Fertil Steril, 83(2005): 1830-1836.
  155. Wurn B.F., Wurn L.J., King C.R., Heuer M.A., Roscow A.S., Hornberger K., Scharf E.S. «Treating fallopian tube occlusion with a manual pelvic physical therapy.» Altern Ther Health Med, 14(2008):18-23.
  156. Wykes C.B. Clark T.J. Khan K.S. «Accuracy of laparoscopy in the diagnosis of endometriosis: a systematic quantitative review.» BJOG, 111(2004):1204-1212.
  157. Xu X., Yin H.,Tang D., Zhang L., Gosden R.G. «Application of traditional Chinese medicine in the treatment of infertility.» Hum Fertil (Camb), 6(2003):161-168.
  158. Zegers-Hochschild F., Adamson G.D., de Mouzon J., Ishihara O., Mansour R., Nygren K., Sullivan E., van der Poel S. «International Committee for Monitoring Assisted Reproductive Technology and World Health Organisation. The International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) Revised Glossary on ART Terminology, 2009.» Hum Reprod, 24(2009):2683-2687.
  159. Zhou J., Qu F. «Treating gynaecological disorders with traditional Chinese medicine: a review.» Afr J Tradit Complement Altern Med, 6(2009):494-517.
  160. Zhu X., Hamilton K.D., McNicol E.D. «Acupuncture for pain in endometriosis.» Cochrane Database Syst Rev (2011):CD007864.

Published

2014-10-20

How to Cite

Dunselman, G., Vermeulen, N., Becker, C., Calhaz-Jorge, C., D’hooghe, T., De Bie, B., Heikinheimo, O., Horne, A., Kiesel, L., Nap, A., Prentice, A., Saridogan, E., Soriano, D., & Nelen, W. (2014). European society of human reproduction and embryology guideline: management of women with endometriosis. REPRODUCTIVE ENDOCRINOLOGY, (19), 54–67. https://doi.org/10.18370/2309-4117.2014.19.54-67

Issue

Section

Clinical guidelines