Display options
Share it on

Hum Reprod Open. 2021 Oct 22;2021(4):hoab025. doi: 10.1093/hropen/hoab025. eCollection 2021.

Endometriosis classification, staging and reporting systems: a review on the road to a universally accepted endometriosis classification.

Human reproduction open

Nathalie Vermeulen, Mauricio S Abrao, Jon I Einarsson, Andrew W Horne, Neil P Johnson, Ted T M Lee, Stacey Missmer, John Petrozza, Carla Tomassetti, Krina T Zondervan, Grigoris Grimbizis, Rudy Leon De Wilde

Affiliations

  1. ESHRE, Central Office, Grimbergen, Belgium.
  2. Disciplina de Ginecologia, Departamento de Obstetricia e Ginecologia, Faculdade de Medicina FMUSP, Universidade de Sao Paulo, Sao Paulo, SP, Brazil.
  3. Gynecologic Division, BP - A Beneficencia Portuguesa de Sao Paulo, Sao Paulo, SP, Brazil.
  4. Division of Minimally Invasive Gynecologic Surgery, Department of Obstetrics and Gynecology, Brigham and Women's Hospital, Boston, MA, USA.
  5. University of Edinburgh, MRC Centre for Reproductive Health, QMRI, Edinburgh, UK.
  6. Repromed Auckland, Remuera, Auckland, New Zealand.
  7. Department of Obstetrics, Gynecology and Reproductive Sciences, Magee Womens Hospital of UPMC, Pittsburgh, PA, USA.
  8. Department of Obstetrics, Gynecology and Reproductive Biology, Michigan State University College of Human Medicine, East Lansing, MI, USA.
  9. Department of Epidemiology, Harvard University T H Chan School of Public Health, Boston, MA, USA.
  10. World Endometriosis Research Foundation, WERF, London, UK.
  11. Department of Obstetrics and Gynecology, Massachusetts General Hospital Fertility Center, Boston, MA, USA.
  12. Department of Obstetrics and Gynaecology, University Hospital Leuven, Leuven University Fertility Centre, Leuven, Belgium.
  13. Nuffield Department of Women's & Reproductive Health, University of Oxford, Oxford Endometriosis CaRe Centre, Oxford, Oxfordshire, UK.
  14. University of Oxford, Wellcome Centre for Human Genetics, Oxford, UK.
  15. 1st Department of Obstetrics and Gynecology, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece.
  16. Carl von Ossietzky Universitat Oldenburg, University Hospital for Gynecology, Oldenburg, Germany.

PMID: 34693032 PMCID: PMC8530712 DOI: 10.1093/hropen/hoab025

Abstract

STUDY QUESTION: Which endometriosis classification, staging and reporting systems have been published and validated for use in clinical practice?

SUMMARY ANSWER: Of the 22 endometriosis classification, staging and reporting systems identified in this historical overview, only a few have been evaluated, in 46 studies, for the purpose for which they were developed.

WHAT IS KNOWN ALREADY: In the field of endometriosis, several classification, staging and reporting systems have been developed.

PARTICIPANTS/MATERIALS SETTING METHODS: A systematic PUBMED literature search was performed. Data were extracted and summarized.

MAIN RESULTS AND THE ROLE OF CHANCE: Twenty-two endometriosis classification, staging and reporting systems have been published between 1973 and 2021, each developed for specific, and different, purposes. There still is no international agreement on how to describe the disease. Studies evaluating the different systems are summarized showing a discrepancy between the intended and the evaluated purpose, and a general lack of validation data confirming a correlation with pain symptoms or quality of life for any of the current systems. A few studies confirm the value of the ENZIAN system for surgical description of deep endometriosis. With regards to infertility, the endometriosis fertility index has been confirmed valid for its intended purpose.

LARGE SCALE DATA: NA.

LIMITATIONS REASONS FOR CAUTION: The literature search was limited to PUBMED. Unpublished classification, staging or reporting systems, or those published in books were not considered.

WIDER IMPLICATIONS OF THE FINDINGS: It can be concluded that there is no international agreement on how to describe endometriosis or how to classify it, and that most classification/staging systems show no or very little correlation with patient outcomes. This overview of existing systems is a first step in working toward a universally accepted endometriosis classification.

STUDY FUNDING/COMPETING INTERESTS: The meetings and activities of the working group were funded by the American Association of Gynecologic Laparoscopists, European Society for Gynecological Endoscopy, European Society of Human Reproduction and Embryology and World Endometriosis Society. A.W.H. reports grant funding from the MRC, NIHR, CSO, Wellbeing of Women, Roche Diagnostics, Astra Zeneca, Ferring, Charles Wolfson Charitable Trust, Standard Life, Consultancy fees from Roche Diagnostics, AbbVie, Nordic Pharma and Ferring, outside the submitted work. In addition, A.W.H. has a patent Serum biomarker for endometriosis pending. N.P.J. reports personal fees from Abbott, Guerbet, Myovant Sciences, Vifor Pharma, Roche Diagnostics, outside the submitted work; he is also President of the World Endometriosis Society and chair of the trust board. S.M. reports grants and personal fees from AbbVie, and personal fees from Roche outside the submitted work. C.T. reports grants, non-financial support and other from Merck SA, non-financial support and other from Gedeon Richter, non-financial support from Ferring Pharmaceuticals, outside the submitted work and without private revenue. K.T.Z. reports grants from Bayer Healthcare, MDNA Life Sciences, Roche Diagnostics Inc, Volition Rx, outside the submitted work; she is also a Board member (Secretary) of the World Endometriosis Society and World Endometriosis Research Foundation, Research Advisory Board member of Wellbeing of Women, UK (research charity), and Chair, Research Directions Working Group, World Endometriosis Society. The other authors had nothing to disclose.

TRIAL REGISTRATION NUMBER: NA.

© The Author(s) 2021. Published by Oxford University Press on behalf of European Society of Human Reproduction and Embryology.

Keywords: classification; endometriosis; infertility; reporting; staging; surgery

References

  1. Fertil Steril. 1977 Sep;28(9):1008-10 - PubMed
  2. Int J Gynaecol Obstet. 2015 Oct;131(1):78-81 - PubMed
  3. Gynecol Surg. 2017;14(1):27 - PubMed
  4. Eur J Obstet Gynecol Reprod Biol. 2017 Dec;219:28-34 - PubMed
  5. Fertil Steril. 2011 Apr;95(5):1574-8 - PubMed
  6. Hum Reprod. 2017 Nov 1;32(11):2243-2249 - PubMed
  7. Fertil Steril. 1979 Dec;32(6):633-4 - PubMed
  8. Hum Reprod. 2017 Feb;32(2):315-324 - PubMed
  9. Hum Reprod Open. 2017 Dec 19;2017(4):hox016 - PubMed
  10. Fertil Steril. 1992 Mar;57(3):691-2 - PubMed
  11. Minerva Ginecol. 2012 Aug;64(4):331-5 - PubMed
  12. BJOG. 2020 Jun;127(7):800-809 - PubMed
  13. Int J Gynaecol Obstet. 1998 Mar;60(3):265-9 - PubMed
  14. Curr Opin Obstet Gynecol. 2011 Aug;23(4):213-20 - PubMed
  15. Hum Reprod. 2003 Jan;18(1):157-61 - PubMed
  16. J Assist Reprod Genet. 1998 Jan;15(1):27-31 - PubMed
  17. Taiwan J Obstet Gynecol. 2014 Jun;53(2):224-6 - PubMed
  18. Quant Imaging Med Surg. 2018 Aug;8(7):709-718 - PubMed
  19. Front Surg. 2019 Jun 07;6:27 - PubMed
  20. Fertil Steril. 2015 Jul;104(1):119-23.e1 - PubMed
  21. Ann Rheum Dis. 2014 Jan;73(1):114-23 - PubMed
  22. Reprod Biol Endocrinol. 2013 Dec 11;11:112 - PubMed
  23. Ultrasound Obstet Gynecol. 2014 Sep;44(3):261-78 - PubMed
  24. Gynecol Obstet Invest. 2014;77(3):180-5 - PubMed
  25. Eur J Radiol. 2015 Apr;84(4):568-74 - PubMed
  26. Ultrasound Obstet Gynecol. 2016 Dec;48(6):786-795 - PubMed
  27. Can Med Assoc J. 1971 Oct 23;105(8):836 passim - PubMed
  28. Arch Gynecol Obstet. 2020 Mar;301(3):699-706 - PubMed
  29. Ginekol Pol. 2014 Jun;85(6):446-50 - PubMed
  30. Fertil Steril. 1982 Aug;38(2):171-6 - PubMed
  31. Hum Reprod Open. 2020 Feb 12;2020(1):hoaa002 - PubMed
  32. Fertil Steril. 2015 Jan;103(1):147-52 - PubMed
  33. Fertil Steril. 1997 May;67(5):817-21 - PubMed
  34. Hum Reprod. 2007 Jan;22(1):266-71 - PubMed
  35. Acta Obstet Gynecol Scand. 2021 Jul;100(7):1165-1175 - PubMed
  36. J Minim Invasive Gynecol. 2019 Mar - Apr;26(3):477-483 - PubMed
  37. Hum Reprod. 2006 Oct;21(10):2679-85 - PubMed
  38. Ann N Y Acad Sci. 2011 Mar;1221:61-9 - PubMed
  39. Chin Med J (Engl). 2017 Aug 20;130(16):1932-1937 - PubMed
  40. Eur J Obstet Gynecol Reprod Biol. 2013 Jan;166(1):99-103 - PubMed
  41. Fertil Steril. 1990 Jun;53(6):994-7 - PubMed
  42. Gynecol Obstet Invest. 2015;79(2):113-8 - PubMed
  43. Fertil Steril. 1978 Aug;30(2):240-2 - PubMed
  44. Fertil Steril. 2014 Nov;102(5):1213-22 - PubMed
  45. Medicine (Baltimore). 2019 Sep;98(39):e16965 - PubMed
  46. J Obstet Gynaecol Res. 2020 Mar;46(3):466-478 - PubMed
  47. Asia Oceania J Obstet Gynaecol. 1993 Dec;19(4):391-9 - PubMed
  48. Yonsei Med J. 2015 Jul;56(4):1079-86 - PubMed
  49. Best Pract Res Clin Obstet Gynaecol. 2018 Aug;51:111-118 - PubMed
  50. Hum Reprod. 2013 May;28(5):1280-8 - PubMed
  51. Hum Reprod. 2017 Sep 1;32(9):1812-1818 - PubMed
  52. Zentralbl Gynakol. 2005 Oct;127(5):275-81 - PubMed
  53. BJOG. 2017 Jan;124(2):220-229 - PubMed
  54. Fertil Steril. 1993 May;59(5):1015-21 - PubMed
  55. N Engl J Med. 2020 Mar 26;382(13):1244-1256 - PubMed
  56. J Minim Invasive Gynecol. 2021 Jan;28(1):57-62 - PubMed
  57. Facts Views Vis Obgyn. 2020 Mar 27;11(4):269-297 - PubMed
  58. Obstet Gynecol. 2012 Jul;120(1):104-12 - PubMed
  59. Arch Gynecol Obstet. 2019 Jul;300(1):109-116 - PubMed
  60. J Minim Invasive Gynecol. 2013 Sep-Oct;20(5):543-6 - PubMed
  61. Fertil Steril. 2010 Oct;94(5):1609-15 - PubMed
  62. Reprod Biomed Online. 2018 Jul;37(1):53-59 - PubMed
  63. Obstet Gynecol. 1973 Jul;42(1):19-25 - PubMed
  64. Gynecol Obstet Fertil Senol. 2019 Mar;47(3):265-272 - PubMed
  65. Hum Reprod. 2017 Sep 1;32(9):1786-1801 - PubMed
  66. Fertil Steril. 1995 May;63(5):1108-10 - PubMed
  67. F1000Res. 2019 Apr 23;8: - PubMed
  68. Fertil Steril. 1981 Feb;35(2):131-7 - PubMed
  69. Gynecol Endocrinol. 2005 Aug;21(2):93-100 - PubMed
  70. Gynecol Obstet Invest. 2006;62(1):48-54 - PubMed
  71. BJOG. 2020 Jan;127(1):107-114 - PubMed
  72. Fertil Steril. 1985 Mar;43(3):351-2 - PubMed
  73. Gynecol Obstet Invest. 2019;84(1):86-93 - PubMed
  74. Ann Rheum Dis. 2010 Sep;69(9):1580-8 - PubMed
  75. J Hum Reprod Sci. 2019 Apr-Jun;12(2):98-103 - PubMed
  76. Hum Reprod. 2014 Aug;29(8):1666-76 - PubMed
  77. Acta Eur Fertil. 1991 Jul-Aug;22(4):209-12 - PubMed
  78. Hum Reprod Open. 2019 Apr 03;2019(2):hoz007 - PubMed
  79. J Turk Ger Gynecol Assoc. 2018 Dec 17;20(3):133-137 - PubMed
  80. Acta Obstet Gynecol Scand. 2013 Jan;92(1):3-7 - PubMed
  81. Gynecol Obstet Fertil. 2003 Mar;31(3):197-206 - PubMed

Publication Types