Endometriosis Classification, Staging and Reporting Systems: A Review on the Road to a Universally Accepted Endometriosis Classification † ‡

Carregando...
Imagem de Miniatura
Citações na Scopus
19
Tipo de produção
article
Data de publicação
2021
Título da Revista
ISSN da Revista
Título do Volume
Editora
ELSEVIER B.V.
Autores
VERMEULEN, N.
EINARSSON, J. I.
HORNE, A. W.
JOHNSON, N. P.
LEE, T. T. M.
MISSMER, S.
PETROZZA, J.
TOMASSETTI, C.
ZONDERVAN, K. T.
Citação
JOURNAL OF MINIMALLY INVASIVE GYNECOLOGY, v.28, n.11, p.1822-1848, 2021
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
Objective: In the field of endometriosis, several classification, staging and reporting systems have been developed. Which endometriosis classification, staging and reporting systems have been published and validated for use in clinical practice? Data sources: A systematic PUBMED literature search was performed. Data were extracted and summarized. Methods of study selection: na Tabulation, integration and results: 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. Conclusion: Of the 22 endometriosis classification, staging and reporting systems identified in this historical overview, only a few have been evaluated for the purpose for which they were developed. The literature search was limited to PUBMED. Unpublished classification, staging or reporting systems, or those published in books were not considered. 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 towards a universally accepted endometriosis classification. © 2021
Palavras-chave
classification, Endometriosis, infertility, reporting, staging, surgery
Referências
  1. Johnson, N.P., Hummelshoj, L., Adamson, G.D., World Endometriosis Society consensus on the classification of endometriosis (2017) Human Reproduction, 32, pp. 315-324
  2. Zegers-Hochschild, F., Adamson, G.D., Dyer, S., The International Glossary on Infertility and Fertility Care, 2017 (2017) Hum Reprod, 32, pp. 1786-1801
  3. Keckstein, J., Becker, C.M., Recommendations for the surgical treatment of endometriosis. Part 2: deep endometriosis †‡¶ (2020) Hum Reprod Open, p. 2020
  4. Saridogan, E., Becker, C.M., Recommendations for the Surgical Treatment of Endometriosis. Part 1: Ovarian Endometrioma¶ (2017) Hum Reprod Open, 2017
  5. Keckstein, J., Becker, C.M., Recommendations for the surgical treatment of endometriosis Part 2: deep endometriosis †‡¶ (2020) Facts Views Vis Obgyn, 11, pp. 269-297
  6. Saridogan, E., Becker, C.M., Recommendations for the surgical treatment of endometriosis-part 1: ovarian endometrioma (2017) Gynecol Surg, 14, p. 27
  7. Zondervan, K.T., Becker, C.M., Missmer, S.A., Endometriosis (2020) N Engl J Med, 382, pp. 1244-1256
  8. Miller-Keane, O.T.M., O'Toole, M.T., Miller-Keane encyclopedia and dictionary of medicine, nursing, and allied health (2005), Elsevier Health Sciences Philadelphia, PA, USA
  9. Acosta, A.A., Buttram, V.C., Jr., Besch, P.K., Malinak, L.R., Franklin, R.R., Vanderheyden, J.D., A proposed classification of pelvic endometriosis (1973) Obstet Gynecol, 42, pp. 19-25
  10. Buttram, V.C., Jr., An expanded classification of endometriosis (1978) Fertil Steril, 30, pp. 240-242
  11. Kistner, R.W., Siegler, A.M., Behrman, S.J., Suggested classification for endometriosis: relationship to infertility (1977) Fertil Steril, 28, pp. 1008-1010
  12. Classification of endometriosis. The American Fertility Society (1979) Fertil Steril, 32, pp. 633-634
  13. American Fertility Society. Revised American Fertility Society classification of endometriosis: 1985 (1985) Fertil Steril, 43, pp. 351-352
  14. American Society for Reproductive Medicine. Revised American Society for Reproductive Medicine classification of endometriosis: 1996 (1997) Fertil Steril, 67, pp. 817-821
  15. Knabben, L., Imboden, S., Fellmann, B., Nirgianakis, K., Kuhn, A., Mueller, M.D., Urinary tract endometriosis in patients with deep infiltrating endometriosis: prevalence, symptoms, management, and proposal for a new clinical classification (2015) Fertil Steril, 103, pp. 147-152
  16. Coccia, M.E., Rizzello, F., Ultrasonographic staging: a new staging system for deep endometriosis (2011) Ann N Y Acad Sci, 1221, pp. 61-69
  17. Chapron, C., Dubuisson, J.B., Chopin, N., [Deep pelvic endometriosis: management and proposal for a “surgical classification”] (2003) Gynecol Obstet Fertil, 31, pp. 197-206
  18. Tuttlies, F., Keckstein, J., Ulrich, U., [ENZIAN-score, a classification of deep infiltrating endometriosis] (2005) Zentralbl Gynakol, 127, pp. 275-281
  19. Keckstein, J., Saridogan, E., Ulrich, U.A., The #Enzian classification: A comprehensive non-invasive and surgical description system for endometriosis (2021) Acta Obstet Gynecol Scand
  20. Becker, C.M., Laufer, M.R., Stratton, P., World Endometriosis Research Foundation Endometriosis Phenome and Biobanking Harmonisation Project: I. Surgical phenotype data collection in endometriosis research (2014) Fertil Steril, 102, pp. 1213-1222
  21. Kurata, S., Ishimaru, T., Masuzaki, H., Yamabe, T., Relationship between the prognosis of conception and the location of pelvic involvement in endometriosis: significance of the TOP (tube, ovary, peritoneum) classification (1993) Asia Oceania J Obstet Gynaecol, 19, pp. 391-399
  22. Chattot, C., Huchon, C., Paternostre, A., Du Cheyron, J., Chouillard, E., Fauconnier, A., ENDORECT: a preoperative score to accurately predict rectosigmoid involvement in patients with endometriosis (2019) Hum Reprod Open, 2019. , hoz007
  23. Lafay Pillet, M.C., Huchon, C., Santulli, P., Borghese, B., Chapron, C., Fauconnier, A., A clinical score can predict associated deep infiltrating endometriosis before surgery for an endometrioma (2014) Hum Reprod, 29, pp. 1666-1676
  24. van der Wat, J., Kaplan, M.D., Roman, H., Da Costa, C., The use of modified virtual colonoscopy to structure a descriptive imaging classification with implied severity for rectogenital and disseminated endometriosis (2013) J Minim Invasive Gynecol, 20, pp. 543-546
  25. Menakaya, U., Reid, S., Lu, C., Gerges, B., Infante, F., Condous, G., Performance of ultrasound-based endometriosis staging system (UBESS) for predicting level of complexity of laparoscopic surgery for endometriosis (2016) Ultrasound Obstet Gynecol, 48, pp. 786-795
  26. Ichikawa, M., Akira, S., Kaseki, H., Watanabe, K., Ono, S., Takeshita, T., Accuracy and clinical value of an adhesion scoring system: A preoperative diagnostic method using transvaginal ultrasonography for endometriotic adhesion (2020) J Obstet Gynaecol Res, 46, pp. 466-478
  27. Riiskjaer, M., Egekvist, A.G., Hartwell, D., Forman, A., Seyer-Hansen, M., Kesmodel, U.S., Bowel Endometriosis Syndrome: a new scoring system for pelvic organ dysfunction and quality of life (2017) Hum Reprod, 32, pp. 1812-1818
  28. Lasmar, B.R., Simoes Abraao, M., Lasmar, R.B., Leon Dewilde, R., Simplified approach to the treatment of endometriosis–ECO system (2012) Minerva Ginecol, 64, pp. 331-335
  29. Lasmar, R.B., Lasmar, B.P., Celeste, R.K., Larbig, A., De Wilde, R.L., Validation of a score to guide endometriosis therapy for the non-specialized gynecologist (2015) Int J Gynaecol Obstet, 131, pp. 78-81
  30. Adamson, G.D., Pasta, D.J., Endometriosis fertility index: the new, validated endometriosis staging system (2010) Fertil Steril, 94, pp. 1609-1615
  31. Bouquet de Joliniere, J., Major, A., Ayoubi, J.M., It Is Necessary to Purpose an Add-on to the American Classification of Endometriosis? This Disease Can Be Compared to a Malignant Proliferation While Remaining Benign in Most Cases. EndoGram® Is a New Profile Witness of Its Evolutionary Potential (2019) Front Surg, 6, p. 27
  32. Candiani, G.B., Vercellini, P., Fedele, L., Laparoscopic ovarian puncture for correct staging of endometriosis (1990) Fertil Steril, 53, pp. 994-997
  33. Canis, M., Pouly, J.L., Wattiez, A., Manhes, H., Mage, G., Bruhat, M.A., Incidence of bilateral adnexal disease in severe endometriosis (revised American Fertility Society [AFS], stage IV): should a stage V be included in the AFS classification? (1992) Fertil Steril, 57, pp. 691-692
  34. Hornstein, M.D., Gleason, R.E., Orav, J., The reproducibility of the revised American Fertility Society classification of endometriosis (1993) Fertil Steril, 59, pp. 1015-1021
  35. Rock, J.A., The revised American Fertility Society classification of endometriosis: reproducibility of scoring. ZOLADEX Endometriosis Study Group (1995) Fertil Steril, 63, pp. 1108-1110
  36. Schliep, K.C., Chen, Z., Stanford, J.B., Endometriosis diagnosis and staging by operating surgeon and expert review using multiple diagnostic tools: an inter-rater agreement study (2017) Bjog, 124, pp. 220-229
  37. Schliep, K.C., Stanford, J.B., Chen, Z., Interrater and intrarater reliability in the diagnosis and staging of endometriosis (2012) Obstet Gynecol, 120, pp. 104-112
  38. Lin, S.Y., Lee, R.K., Hwu, Y.M., Lin, M.H., Reproducibility of the revised American Fertility Society classification of endometriosis using laparoscopy or laparotomy (1998) Int J Gynaecol Obstet, 60, pp. 265-269
  39. Tomassetti, C., Bafort, C., Meuleman, C., Welkenhuysen, M., Fieuws, S., D'Hooghe, T., Reproducibility of the Endometriosis Fertility Index: a prospective inter-/intra-rater agreement study (2020) Bjog, 127, pp. 107-114
  40. 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 classification system (2006) Hum Reprod, 21, pp. 2679-2685
  41. Milingos, S., Protopapas, A., Kallipolitis, G., Endometriosis in patients with chronic pelvic pain: is staging predictive of the efficacy of laparoscopic surgery in pain relief? (2006) Gynecol Obstet Invest, 62, pp. 48-54
  42. Nicolaus, K., Zschauer, S., Bräuer, D., Extensive endometriosis surgery: rASRM and Enzian score independently relate to post-operative complication grade (2020) Arch Gynecol Obstet, 301, pp. 699-706
  43. Posadzka, E., Jach, R., Pitynski, K., Nocun, A., Ovarian reserve assessment in women with different stages of pelvic endometriosis (2014) Ginekol Pol, 85, pp. 446-450
  44. Yun, B.H., Jeon, Y.E., Chon, S.J., The Prognostic Value of Individual Adhesion Scores from the Revised American Fertility Society Classification System for Recurrent Endometriosis (2015) Yonsei Med J, 56, pp. 1079-1086
  45. Guzick, D.S., Bross, D.S., Rock, J.A., Assessing the efficacy of The American Fertility Society's classification of endometriosis: application of a dose-response methodology (1982) Fertil Steril, 38, pp. 171-176
  46. Rock, J.A., Guzick, D.S., Sengos, C., Schweditsch, M., Sapp, K.C., Jones, H.W., Jr, The conservative surgical treatment of endometriosis: evaluation of pregnancy success with respect to the extent of disease as categorized using contemporary classification systems (1981) Fertil Steril, 35, pp. 131-137
  47. Pal, L., Shifren, J.L., Isaacson, K.B., Chang, Y., Leykin, L., Toth, T.L., Impact of varying stages of endometriosis on the outcome of in vitro fertilization-embryo transfer (1998) J Assist Reprod Genet, 15, pp. 27-31
  48. Barbosa, M.A., Teixeira, D.M., Navarro, P.A., Ferriani, R.A., Nastri, C.O., Martins, W.P., Impact of endometriosis and its staging on assisted reproduction outcome: systematic review and meta-analysis (2014) Ultrasound Obstet Gynecol, 44, pp. 261-278
  49. Pop-Trajkovic, S., Popovic, J., Antic, V., Radovic, D., Stefanovic, M., Vukomanovic, P., Stages of endometriosis: does it affect in vitro fertilization outcome (2014) Taiwan J Obstet Gynecol, 53, pp. 224-226
  50. Vercellini, P., Fedele, L., Aimi, G., Pietropaolo, G., Consonni, D., Crosignani, P.G., Association between endometriosis stage, lesion type, patient characteristics and severity of pelvic pain symptoms: a multivariate analysis of over 1000 patients (2007) Hum Reprod, 22, pp. 266-271
  51. Szendei, G., Hernadi, Z., Devenyi, N., Csapo, Z., Is there any correlation between stages of endometriosis and severity of chronic pelvic pain? Possibilities of treatment (2005) Gynecol Endocrinol, 21, pp. 93-100
  52. Marana, R., Muzii, L., Caruana, P., Dell'Acqua, S., Mancuso, S., Evaluation of the correlation between endometriosis extent, age of the patients and associated symptomatology (1991) Acta Eur Fertil, 22, pp. 209-212
  53. Kim, J.S., Lee, C.W., Yun, J., Use of the Endometriosis Fertility Index to Predict Natural Pregnancy after Endometriosis Surgery: A Single-Center Study (2019) Gynecol Obstet Invest, 84, pp. 86-93
  54. Boujenah, J., Bonneau, C., Hugues, J.N., Sifer, C., Poncelet, C., External validation of the Endometriosis Fertility Index in a French population (2015) Fertil Steril, 104, pp. 119-123. , e111
  55. Boujenah, J., Cedrin-Durnerin, I., Herbemont, C., Bricou, A., Sifer, C., Poncelet, C., Use of the endometriosis fertility index in daily practice: A prospective evaluation (2017) Eur J Obstet Gynecol Reprod Biol, 219, pp. 28-34
  56. Garavaglia, E., Pagliardini, L., Tandoi, I., External validation of the endometriosis fertility index (EFI) for predicting spontaneous pregnancy after surgery: further considerations on its validity (2015) Gynecol Obstet Invest, 79, pp. 113-118
  57. Li, X., Zeng, C., Zhou, Y.F., Endometriosis Fertility Index for Predicting Pregnancy after Endometriosis Surgery (2017) Chin Med J (Engl), 130, pp. 1932-1937
  58. Maheux-Lacroix, S., Nesbitt-Hawes, E., Deans, R., Endometriosis fertility index predicts live births following surgical resection of moderate and severe endometriosis (2017) Hum Reprod, 32, pp. 2243-2249
  59. 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 (2013) Hum Reprod, 28, pp. 1280-1288
  60. Wang, W., Li, R., Fang, T., Endometriosis fertility index score maybe more accurate for predicting the outcomes of in vitro fertilisation than r-AFS classification in women with endometriosis (2013) Reprod Biol Endocrinol, 11, p. 112
  61. Zeng, C., Xu, J.N., Zhou, Y., Zhou, Y.F., Zhu, S.N., Xue, Q., Reproductive performance after surgery for endometriosis: predictive value of the revised American Fertility Society classification and the endometriosis fertility index (2014) Gynecol Obstet Invest, 77, pp. 180-185
  62. Zhang, X., Liu, D., Huang, W., Wang, Q., Feng, X., Tan, J., Prediction of Endometriosis Fertility Index in patients with endometriosis-associated infertility after laparoscopic treatment (2018) Reprod Biomed Online, 37, pp. 53-59
  63. Negi, N., Roy, K.K., Kumar, S., Nair, V.G., Vanamail, P., Clinical Outcome Analysis and Correlation of Reproductive Outcome with Endometriosis Fertility Index in Laparoscopically Managed Endometriosis Patients: A Retrospective Cohort Study (2019) J Hum Reprod Sci, 12, pp. 98-103
  64. Zhou, Y., Lin, L., Chen, Z., Fertility performance and the predictive value of the endometriosis fertility index staging system in women with recurrent endometriosis: A retrospective study (2019) Medicine (Baltimore), 98, p. e16965
  65. Vesali, S., Razavi, M., Rezaeinejad, M., Maleki-Hajiagha, A., Maroufizadeh, S., Sepidarkish, M., Endometriosis Fertility Index for predicting non-assisted reproductive technology pregnancy after endometriosis surgery: a systematic review and meta-analysis (2020) Bjog
  66. Chaabane, S., Nguyen Xuan, H.T., Paternostre, A., [Endometriosis: Assessment of the Ultrasound-Based Endometriosis Staging System score (UBESS) in predicting surgical difficulty] (2019) Gynecol Obstet Fertil Senol, 47, pp. 265-272
  67. Espada, M., Leonardi, M., Aas-Eng, K., A Multicenter International Temporal and External Validation Study of the Ultrasound-based Endometriosis Staging System (2020) J Minim Invasive Gynecol
  68. Tompsett, J., Leonardi, M., Gerges, B., Ultrasound-Based Endometriosis Staging System: Validation Study to Predict Complexity of Laparoscopic Surgery (2019) J Minim Invasive Gynecol, 26, pp. 477-483
  69. Haas, D., Chvatal, R., Habelsberger, A., Wurm, P., Schimetta, W., Oppelt, P., Comparison of revised American Fertility Society and ENZIAN staging: a critical evaluation of classifications of endometriosis on the basis of our patient population (2011) Fertil Steril, 95, pp. 1574-1578
  70. Morgan-Ortiz, F., Lopez-de la Torre, M.A., Lopez-Zepeda, M.A., Morgan-Ruiz, F.V., Ortiz-Bojorquez, J.C., Bolivar-Rodriguez, M.A., Clinical characteristics and location of lesions in patients with deep infiltrating endometriosis: using the revised Enzian classification (2018) J Turk Ger Gynecol Assoc
  71. Burla, L., Scheiner, D., Samartzis, E.P., The ENZIAN score as a preoperative MRI-based classification instrument for deep infiltrating endometriosis (2019) Arch Gynecol Obstet
  72. Di Paola, V., Manfredi, R., Castelli, F., Negrelli, R., Mehrabi, S., Pozzi Mucelli, R., Detection and localization of deep endometriosis by means of MRI and correlation with the ENZIAN score (2015) Eur J Radiol, 84, pp. 568-574
  73. Haas, D., Chvatal, R., Habelsberger, A., Preoperative planning of surgery for deeply infiltrating endometriosis using the ENZIAN classification (2013) Eur J Obstet Gynecol Reprod Biol, 166, pp. 99-103
  74. Aletaha, D., Neogi, T., Silman, A.J., 2010 rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative (2010) Ann Rheum Dis, 69, pp. 1580-1588
  75. Radner, H., Neogi, T., Smolen, J.S., Aletaha, D., Performance of the 2010 ACR/EULAR classification criteria for rheumatoid arthritis: a systematic literature review (2014) Ann Rheum Dis, 73, pp. 114-123
  76. Denoix, P., Nomenclature classification des cancers (1952) Bull Inst Nat Hyg(Paris), 7, pp. 743-748
  77. Sellers, A.H., The clinical classification of malignant tumours: the TNM system (1971) Can Med Assoc J, 105, p. 836. , passim
  78. Edge, S.B., Byrd, D.R., Carducci, M.A., Compton, C.C., Fritz, A., Greene, F., AJCC cancer staging manual (2010), Springer New York
  79. Lim, W., Ridge, C.A., Nicholson, A.G., The, M.S., 8(th) lung cancer TNM classification and clinical staging system: review of the changes and clinical implications (2018) Quant Imaging Med Surg, 8, pp. 709-718
  80. Haas, D., Shebl, O., Shamiyeh, A., Oppelt, P., The rASRM score and the Enzian classification for endometriosis: their strengths and weaknesses (2013) Acta Obstet Gynecol Scand, 92, pp. 3-7
  81. Andres, M.P., Borrelli, G.M., Abrao, M.S., Endometriosis classification according to pain symptoms: can the ASRM classification be improved? (2018) Best Pract Res Clin Obstet Gynaecol, 51, pp. 111-118
  82. Adamson, G.D., Endometriosis classification: an update (2011) Curr Opin Obstet Gynecol, 23, pp. 213-220
  83. Rolla, E., Endometriosis: advances and controversies in classification, pathogenesis, diagnosis, and treatment (2019) F1000Res, 8