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Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities

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Nisolle, Michelle [UCL] Donnez, Jacques [UCL]

OBJECTIVE: To review the histogenesis of peritoneal, ovarian, and rectovaginal endometriotic lesions. DESIGN: The comparison of morphologic, morphometric, and histochemical data observed in each type of lesion. SETTING: A university hospital department of gynecology. PATIENT(S): Patients complaining of infertility or pelvic pain with laparoscopically proved endometriosis. INTERVENTION(S): Laparoscopy was performed, and biopsy specimens from the endometriotic lesions were histologically studied. RESULT(S): Three types of endometriotic lesions must be considered: peritoneal, ovarian, and rectovaginal. Morphologic and morphometric data show similarities between eutopic endometrium and red peritoneal lesions, suggesting that these lesions are the first stage of early implantation of endometrial glands and stroma. After partial shedding, the red lesions regrow constantly. The shedding induces an inflammatory reaction, provoking scarification, and the lesions become black. The subsequent fibrosis leads to areas of white opacification that are inactive. The pathogenesis of ovarian endometriomas is a source of controversy. Although there seems to be a consensus concerning the invagination theory, there is still a contradiction between the implantation theory and the metaplasia theory. We recently showed that the mesothelium covering the ovary can invaginate into the ovarian cortex, pushing back the primordial follicles. The presence of mesothelial invagination in continuum with endometriotic tissue suggests that metaplastic histogenesis of ovarian endometriotic lesions occurs. Rectovaginal endometriotic nodules must be considered adenomyomas, consisting of smooth muscle with active glandular epithelium and scanty stroma. Immunocytochemical results show poor differentiation and hormonal independence of these lesions and indicate a close relation with their mesodermal müllerian origin. CONCLUSION(S): Peritoneal, ovarian and rectovaginal endometriotic lesions must be considered as three separate entities with different pathogeneses.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 1997
Journal information "Fertility and Sterility" - Vol. 68, no. 4, p. 585-596 (1997)
Peer reviewed yes
Publisher Elsevier Inc. (Philadelphia)
issn 0015-0282
e-issn 1556-5653
Publication status Publié
Affiliations UCL - MD/GYPE - Département de gynécologie, d'obstétrique et de pédiatrie
UCL - (SLuc) Service de gynécologie et d'andrologie
MESH Subject Endometriosis - pathology ; Female ; Humans ; Ovarian Diseases - pathology ; Peritoneal Diseases - pathology ; Rectal Diseases - pathology ; Vaginal Diseases - pathology
Keywords Endometriosis ; Peritoneum ; Ovary ; Rectovaginal nodule ; Histogenesis
Links
  1. Donnez Jacques, Nisolle Michèle, Casanas-Roux Françoise, Three-dimensional architectures of peritoneal endometriosis**Supported in part by Fonds de la Recherche Scientifique Médicale grant no 3.4587.90, Brussels, Belgium., 10.1016/s0015-0282(16)55012-2
  2. Donnez Jacques, Nisolle Michelle, Smoes Pierre, Gillet Nadine, Beguin Sandrine, Casanas-Roux Françoise, Peritoneal endometriosis and “endometriotic” nodules of the rectovaginal septum are two different entities**Supported by Fonds de la Recherche Scientifique, grant no. 3.4587.90, Brussels, Belgium and a grant from Ipsen Biotech, Paris, France., 10.1016/s0015-0282(16)58501-x
  3. Nisolle Michelle, Donnez Jacques, Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities, 10.1016/s0015-0282(97)00191-x
  4. Von Rokitansky, Zeitschr Gesellsch Aerzte Wien, 37, 577 (1860)
  5. Sampson John A., Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity, 10.1016/s0002-9378(15)30003-x
  6. Halme, Obstet Gynecol, 64, 151 (1984)
  7. Jenkins, Obstet Gynecol, 67, 335 (1986)
  8. Kruitwagen Roy F.P.M., Poels Lambert G., Willemsen Wim N.P., Jap Paul H.K., Thomas Chris M.G., Rolland Rune, Retrograde seeding of endometrial epithelial cells by uterine-tubal flushing, 10.1016/s0015-0282(16)54533-6
  9. Koks Carolien A.M., Dunselman Gerard A.J., de Goeij Anton F.P.M., Arends Jan Willem, Evers Johannes L.H., Evaluation of a menstrual cup to collect shed endometrium for in vitro studies, 10.1016/s0015-0282(97)00250-1
  10. Sanfilippo Joseph S., Wakim Najib G., Schikler Kenneth N., Yussman Marvin A., Endometriosis in association with uterine anomaly, 10.1016/0002-9378(86)90389-3
  11. Darrow Sherri L., Vena John E., Batt Ronald E., Zielezny Maria A., Michalek Arthur M., Selman Sharon, Menstrual Cycle Characteristics and the Risk of Endometriosis : , 10.1097/00001648-199303000-00009
  12. VERCELLINI P, DEGIORGI O, AIMI G, PANAZZA S, UGLIETTI A, CROSIGNANI P, Menstrual characteristics in women with and without endometriosis, 10.1016/s0029-7844(97)00235-4
  13. Arumugam Kulenthran, Lim Jason M. H., Menstrual characteristics associated with endometriosis, 10.1111/j.1471-0528.1997.tb14357.x
  14. Spuijbroek Marleen D.E.H., Dunselman Gerard A.J., Menheere Paul P.C.A., Evers Johannes L.H., Early endometriosis invades the extracellular matrix, 10.1016/s0015-0282(16)55437-5
  15. Lousse Jean-Christophe, Defrère Sylvie, Van Langendonckt Anne, Gras Jérémie, González-Ramos Reinaldo, Colette Sébastien, Donnez Jacques, Iron storage is significantly increased in peritoneal macrophages of endometriosis patients and correlates with iron overload in peritoneal fluid, 10.1016/j.fertnstert.2008.02.103
  16. Lousse, J Endometr, 1, 19 (2009)
  17. Haney A.F., Muscato Joseph J., Weinberg J. Brice, Peritoneal fluid cell populations in infertility patients, 10.1016/s0015-0282(16)45567-6
  18. Hill Joseph A., Faris Heidi M.P., Schiff Isaac, Anderson Deborah J., Characterization of leukocyte subpopulations in the peritoneal fluid of women with endometriosis**Supported by grants CA42738, HD00815-01, and HD23547-01, from the United States Public Health Service, Bethesda, Maryland; by the 1987–88 American Fertility Society—Ortho Distinguished Fellowship Award; and by the Fearing Laboratory Endowment.††Presented at the Forty-Third Annual Meeting of the American Fertility Society, Reno, Nevada, September 28 to 30, 1987., 10.1016/s0015-0282(16)60062-6
  19. SONG M, Presence of endometrial epithelial cells in the peritoneal cavity and the mesothelial inflammatory response*1, 10.1016/s0015-0282(02)04836-7
  20. Cao Xuan, Yang DongZi, Song MingQing, Murphy Ana, Parthasarathy Sampath, The presence of endometrial cells in the peritoneal cavity enhances monocyte recruitment and induces inflammatory cytokines in mice: Implications for endometriosis, 10.1016/j.fertnstert.2004.04.040
  21. Donnez Jacques, Van Langendonckt Anne, Typical and subtle atypical presentations of endometriosis : , 10.1097/00001703-200410000-00013
  22. Vinatier D., Orazi G., Cosson M., Dufour P., Theories of endometriosis, 10.1016/s0301-2115(00)00405-x
  23. Oosterlynck Didier J., Cornillie Freddy J., Waer Mark, Vandeputte Michel, Koninckx Philippe R., Women with endometriosis show a defect in natural killer activity resulting in a decreased cytotoxicity to autologous endometrium**Supported by the National Fund for Scientific Research, Brussels, Belgium., 10.1016/s0015-0282(16)54414-8
  24. Vigano P, Expression of intercellular adhesion molecule (ICAM)-1 mRNA and protein is enhanced in endometriosis versus endometrial stromal cells in culture, 10.1093/molehr/4.12.1150
  25. van der Linden Paul J.Q., de Goeij Anton F.P.M., Dunselman Gerard A.J., Erkens Heleen W.H., Evers Johannes L.H., Endometrial cell adhesion in an in vitro model using intact amniotic membranes**Supported in part by research grants from Ipsen Biotech, Paris, France and from Organon International B.V., Oss, The Netherlands., 10.1016/s0015-0282(16)58030-3
  26. Groothuis P. G., Koks C. A., de Goeij A. F., Dunselman G. A., Arends J. W., Evers J. L., Adhesion of human endometrium to the epithelial lining and extracellular matrix of amnion in vitro: an electron microscopic study, 10.1093/humrep/13.8.2275
  27. Groothuis Patrick G, Koks Carolien A.M, de Goeij Anton F.P.M, Dunselman Gerard A.J, Arends Jan Willem, Evers Johannes L.H, Adhesion of human endometrial fragments to peritoneum in vitro, 10.1016/s0015-0282(99)00122-3
  28. WITZ C, MONOTOYARODRIGUEZ I, SCHENKEN R, Whole explants of peritoneum and endometrium: a novel model of the early endometriosis lesion, 10.1016/s0015-0282(98)00400-2
  29. Witz Craig A, Thomas Mika R, Montoya-Rodriguez Iris A, Nair Anitha S, Centonze Victoria E, Schenken Robert S, Short-term culture of peritoneum explants confirms attachment of endometrium to intact peritoneal mesothelium, 10.1016/s0015-0282(00)01699-x
  30. Debrock S., In-vitro adhesion of endometrium to autologous peritoneal membranes: effect of the cycle phase and the stage of endometriosis, 10.1093/humrep/17.10.2523
  31. Zhang Ren-jie, Wild Robert A., Ojago James M., Effect of tumor necrosis factor-α on adhesion of human endometrial stromal cells to peritoneal mesothelial cells: an in vitro system**Presented at the 39th Annual Meeting of the Society for Gynecologic Investigation, San Antonio, Texas, March 18 to 21, 1992., 10.1016/s0015-0282(16)55976-7
  32. Wild, J Soc Gynecol Invent, 1, 165 (1994)
  33. Lucidi R. Scott, Witz Craig A., Chrisco Michelle, Binkley Peter A., Shain Sydney A., Schenken Robert S., A novel in vitro model of the early endometriotic lesion demonstrates that attachment of endometrial cells to mesothelial cells is dependent on the source of endometrial cells, 10.1016/j.fertnstert.2004.10.058
  34. Debrock Sophie, De Strooper Bart, Perre Sarah Vander, Hill Joseph A., D’Hooghe Thomas M, Tumour necrosis factor-α, interleukin-6 and interleukin-8 do not promote adhesion of human endometrial epithelial cells to mesothelial cells in a quantitative in vitro model*, 10.1093/humrep/dei375
  35. Nisolle Michelle, Casanas-Roux Françoise, Donnez Jacques, Early-stage endometriosis: adhesion and growth of human menstrual endometrium in nude mice, 10.1016/s0015-0282(00)00601-4
  36. WITZ CRAIG A., DECHAUD HERVE, MONTOYA-RODRIGUEZ IRIS A., THOMAS MIKA R., NAIR ANITHA S., CENTONZE VICTORIA E., SCHENKEN ROBERT S., AnIn VitroModel to Study the Pathogenesis of the Early Endometriosis Lesion, 10.1111/j.1749-6632.2002.tb02790.x
  37. van der Linden Paul J.Q., de Goeif Anton F.P.M., Dunselman Gerard A.J., Arend Jan Willem, Evers Johannes L.H., P-Cadherin Expression in Human Endometrium and Endometriosis, 10.1159/000292475
  38. van der Linden Paul J.Q., de Goeij Anton F.P.M., Dunselman Gerard A.J., Erkens Heleen W.H., Evers Johannes L.H., Expression of cadherins and integrins in human endometrium throughout the menstrual cycle**Supported in part by a research grant from Organon International B.V., Oss, The Netherlands., 10.1016/s0015-0282(16)57599-2
  39. Bridges J. E., Prentice A., Roche W., Englefield P., Thomas E. J., Expression of integrin adhesion molecules in endometrium and endometriosis, 10.1111/j.1471-0528.1994.tb13187.x
  40. Kim Lawrence T., Yamada Kenneth M., Evidence That β1 Integrins in Keratinocyte Cell–Cell Junctions Are Not in the Ligand-Occupied Conformation, 10.1111/1523-1747.ep12292589
  41. Regidor P., Expression pattern of integrin adhesion molecules in endometriosis and human endometrium, 10.1093/humupd/4.5.710
  42. Cell Adhesion Molecules and Endometriosis, 10.1055/s-2003-41324
  43. Yaegashi Nobuo, Fujita Nobuhiro, Yajima Akira, Nakamura Masataka, Menstrual cycle dependent expression of CD44 in normal human endometrium, 10.1016/0046-8177(95)90008-x
  44. Dechaud Herve, Witz Craig A., Montoya-Rodriguez Iris A., Degraffenreid Linda A., Schenken Robert S., Mesothelial cell–associated hyaluronic acid promotes adhesion of endometrial cells to mesothelium, 10.1016/s0015-0282(01)02839-4
  45. Yung, Am J Pathol, 146, 520 (1995)
  46. Rodgers W H, Matrisian L M, Giudice L C, Dsupin B, Cannon P, Svitek C, Gorstein F, Osteen K G, Patterns of matrix metalloproteinase expression in cycling endometrium imply differential functions and regulation by steroid hormones., 10.1172/jci117461
  47. Witz Craig A, Cho Sook, Montoya-Rodriguez Iris A, Schenken Robert S, The α2β1 and α3β1 integrins do not mediate attachment of endometrial cells to peritoneal mesothelium, 10.1016/s0015-0282(02)03340-x
  48. WITZ C, Time series analysis of transmesothelial invasion by endometrial stromal and epithelial cells using three-dimensional confocal microscopy, 10.1016/s0015-0282(02)04834-3
  49. Dunselman Gerard A.J., Groothuis Patrick G., de Goeij Anton F.P.M., Evers Johannes L.H., The Mesothelium, Teflon or Velcro?, 10.1093/humrep/16.4.605
  50. Marbaix E., Kokorine I., Moulin P., Donnez J., Eeckhout Y., Courtoy P. J., Menstrual breakdown of human endometrium can be mimicked in vitro and is selectively and reversibly blocked by inhibitors of matrix metalloproteinases., 10.1073/pnas.93.17.9120
  51. Singer C. F., Marbaix E., Kokorine I., Lemoine P., Donnez J., Eeckhout Y., Courtoy P. J., Paracrine stimulation of interstitial collagenase (MMP-1) in the human endometrium by interleukin 1  and its dual block by ovarian steroids, 10.1073/pnas.94.19.10341
  52. HENRIET PATRICK, CORNET PATRICIA B., LEMOINE PASCALE, GALANT CHRISTINE, SINGER CHRISTIAN F., COURTOY PIERRE J., EECKHOUT YVES, MARBAIX ETIENNE, Circulating Ovarian Steroids and Endometrial Matrix Metalloproteinases (MMPs), 10.1111/j.1749-6632.2002.tb02773.x
  53. Malik, J Immunol, 156, 3952 (1996)
  54. Schonbeck U., Mach F., Sukhova G. K., Murphy C., Bonnefoy J.-Y., Fabunmi R. P., Libby P., Regulation of Matrix Metalloproteinase Expression in Human Vascular Smooth Muscle Cells by T Lymphocytes : A Role for CD40 Signaling in Plaque Rupture?, 10.1161/01.res.81.3.448
  55. Osteen Kevin, Bruner Kaylon, Sharpe-Timms Kathy, Steroid and Growth Factor Regulation of Matrix Metalloproteinase Expression and Endometriosis, 10.1055/s-2007-1016334
  56. Sillem M, Extracellular matrix remodelling in the endometrium and its possible relevance to the pathogenesis of endometriosis, 10.1093/humupd/4.5.730
  57. SHARPE-TIMMS KATHY L., COX KATHRYN E., Paracrine Regulation of Matrix Metalloproteinase Expression in Endometriosis, 10.1111/j.1749-6632.2002.tb02775.x
  58. Kokorine Isabelle, Nisolle Michelle, Donnez Jacques, Eeckhout Yves, Courtoy Pierre J., Marbaix Etienne, Expression of interstitial collagenase (matrix metalloproteinase-1) is related to the activity of human endometriotic lesions, 10.1016/s0015-0282(97)81510-5
  59. Bruner K L, Matrisian L M, Rodgers W H, Gorstein F, Osteen K G, Suppression of matrix metalloproteinases inhibits establishment of ectopic lesions by human endometrium in nude mice., 10.1172/jci119478
  60. Nisolle Michelle, Casanas-Roux Françoise, Marbaix Etienne, Jadoul Pascale, Donnez Jacques, Transplantation of cultured explants of human endometrium into nude mice, 10.1093/humrep/15.3.572
  61. Harada Tasuku, Iwabe Tomio, Terakawa Naoki, Role of cytokines in endometriosis, 10.1016/s0015-0282(01)01816-7
  62. Khan Khaleque Newaz, Masuzaki Hideaki, Fujishita Akira, Kitajima Michio, Sekine Ichiro, Ishimaru Tadayuki, Immunoexpression of hepatocyte growth factor and c-Met receptor in the eutopic endometrium predicts the activity of ectopic endometrium, 10.1016/s0015-0282(02)04535-1
  63. Apoptosis and the Pathogenesis of Endometriosis, 10.1055/s-2003-41323
  64. Béliard Aude, Noël Agnès, Foidart Jean-Michel, Reduction of apoptosis and proliferation in endometriosis, 10.1016/j.fertnstert.2003.11.048
  65. Donnez J., Smoes P., Gillerot S., Casanas-Roux F., Nisolle M., Vascular endothelial growth factor (VEGF) in endometriosis, 10.1093/humrep/13.6.1686
  66. Groothuis P.G., Nap A.W., Winterhager E., Grümmer R., Vascular development in endometriosis, 10.1007/s10456-005-9005-x
  67. Folkman, J Biol Chem, 267, 10931 (1992)
  68. Oosterlynck Didier J., Meuleman Christel, Sobis Halina, Vandeputte Michel, Koninckx Philippe R., Angiogenic activity of peritoneal fluid from women with endometriosis**Supported by the National Fund for Scientific Research, Brussels, Belgium., 10.1016/s0015-0282(16)55859-2
  69. Koninckx P., Endometriotic disease: the role of peritoneal fluid, 10.1093/humupd/4.5.741
  70. McLaren J., Vascular endothelial growth factor and endometriotic angiogenesis, 10.1093/humupd/6.1.45
  71. McLaren J., Prentice A., Charnock-Jones D.S., Smith S.K., Vascular endothelial growth factor (VEGF) concentrations are elevated in peritoneal fluid of women with endometriosis, 10.1093/oxfordjournals.humrep.a019023
  72. Shifren J. L., Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis, 10.1210/jc.81.8.3112
  73. Dabrosin Charlotta, Gyorffy Steve, Margetts Peter, Ross Catherine, Gauldie Jack, Therapeutic Effect of Angiostatin Gene Transfer in a Murine Model of Endometriosis, 10.1016/s0002-9440(10)64251-4
  74. Hull M. Louise, Charnock-Jones D. Stephen, Chan Clement L. K., Bruner-Tran Kaylon L., Osteen Kevin G., Tom Brian D. M., Fan Tai-Ping D., Smith Stephen K., Antiangiogenic Agents Are Effective Inhibitors of Endometriosis, 10.1210/jc.2002-021912
  75. Nap Annemiek W., Griffioen Arjan W., Dunselman Gerard A. J., Bouma-Ter Steege Jessica C. A., Thijssen Victor L. J. L., Evers Johannes L. H., Groothuis Patrick G., Antiangiogenesis Therapy for Endometriosis, 10.1210/jc.2003-031406
  76. Van Langendonckt A., Donnez J., Defrere S., Dunselman G. A.J., Groothuis P. G., Antiangiogenic and vascular-disrupting agents in endometriosis: pitfalls and promises, 10.1093/molehr/gan019
  77. Van Langendonckt A., Characterization of iron deposition in endometriotic lesions induced in the nude mouse model, 10.1093/humrep/deh182
  78. González-Ramos Reinaldo, Donnez Jacques, Defrère Sylvie, Leclercq Isabelle, Squifflet Jean, Lousse Jean-Christophe, Van Langendonckt Anne, Nuclear factor-kappa B is constitutively activated in peritoneal endometriosis, 10.1093/molehr/gam033
  79. Nisolle, Fertil Steril, 59, 681 (1993)
  80. Ridley John H., Edwards I. Keith, Experimental endometriosis in the human, 10.1016/0002-9378(58)90011-5
  81. Oliker, J Urol, 106, 858 (1971)
  82. Schrodt, J Urol, 124, 722 (1980)
  83. Schifrin Barry S., Erez Selcuk, Moore J. George, Teen-age endometriosis, 10.1016/s0002-9378(16)33845-5
  84. Cassina Paolo Claudio, Weder Walter, Hauser Markus, Kacl Georg, Imthurn Bruno, Schröder Sören, Catamenial Hemoptysis, 10.1378/chest.111.5.1447
  85. Olive, Obstet Gynecol, 69, 412 (1987)
  86. Von Recklinghausen, Wien Klin Wochenschr, 8, 530 (1896)
  87. Sampson John A., Heterotopic or misplaced endometrial tissue, 10.1016/s0002-9378(25)90629-1
  88. Hobbs John E., Bortnick A.R., Endometriosis of the Lungs, 10.1016/s0002-9378(15)30807-3
  89. Chan Rachel W.S., Schwab Kjiana E., Gargett Caroline E., Clonogenicity of Human Endometrial Epithelial and Stromal Cells1, 10.1095/biolreprod.103.024109
  90. Schwab Kjiana Elkje, Chan Rachel Wah Shan, Gargett Caroline Eve, Putative stem cell activity of human endometrial epithelial and stromal cells during the menstrual cycle, 10.1016/j.fertnstert.2005.02.056
  91. Taylor Hugh S., Vanden Heuvel Gregory B., Igarashi Peter, A Conserved Hox Axis in the Mouse and Human Female Reproductive System: Late Establishment and Persistent Adult Expression of the Hoxa Cluster Genes, 10.1095/biolreprod57.6.1338
  92. Du Hongling, Taylor Hugh S., Contribution of Bone Marrow-Derived Stem Cells to Endometrium and Endometriosis, 10.1634/stemcells.2006-0828
  93. Gargett C.E., Uterine stem cells: What is the evidence?, 10.1093/humupd/dml045
  94. Sasson Isaac E., Taylor Hugh S., Stem Cells and the Pathogenesis of Endometriosis, 10.1196/annals.1434.014
  95. Leyendecker G., Endometriosis results from the dislocation of basal endometrium, 10.1093/humrep/17.10.2725
  96. Giudice Linda C, Kao Lee C, Endometriosis, 10.1016/s0140-6736(04)17403-5
  97. Montgomery Grant W., Nyholt Dale R., Zhao Zhen Zhen, Treloar Susan A., Painter Jodie N., Missmer Stacey A., Kennedy Stephen H., Zondervan Krina T., The search for genes contributing to endometriosis risk, 10.1093/humupd/dmn016
  98. SIMPSON JOE LEIGH, BISCHOFF FARIDEH Z., Heritability and Molecular Genetic Studies of Endometriosis, 10.1111/j.1749-6632.2002.tb02785.x
  99. Guo S.-W., Epigenetics of endometriosis, 10.1093/molehr/gap064
  100. Rier S, Endometriosis in Rhesus Monkeys (Macaca mulatta) Following Chronic Exposure to 2,3,7,8-Tetrachlorodibenzo-p-dioxin, 10.1006/faat.1993.1119
  101. Heilier Jean-François, Nackers Fabienne, Verougstraete Violaine, Tonglet René, Lison Dominique, Donnez Jacques, Increased dioxin-like compounds in the serum of women with peritoneal endometriosis and deep endometriotic (adenomyotic) nodules, 10.1016/j.fertnstert.2005.04.001
  102. Bulun Serdar E., Endometriosis, 10.1056/nejmra0804690
  103. Attar E., Bulun S.E., Aromatase and other steroidogenic genes in endometriosis: translational aspects, 10.1093/humupd/dmi034
  104. Colette S., Lousse J.C., Defrere S., Curaba M., Heilier J.F., Van Langendonckt A., Mestdagt M., Foidart J.M., Loumaye E., Donnez J., Absence of aromatase protein and mRNA expression in endometriosis, 10.1093/humrep/dep199
  105. Colette, N Engl J Med, 306, 1911 (2009)
  106. Colette S., Donnez J., Aromatase et endométriose : mythe ou réalité ?, 10.1016/j.gyobfe.2010.03.014
  107. Nisolle Michelle, Casanas-Roux Françoise, Anaf Vincent, Mine Jean-Michel, Donnez Jacques, Morphometric study of the stromal vascularization in peritoneal endometriosis**Supported in part by Fonds de la Recherche Scientifique Médicale, grant 3.4587.90, Brussels, Belgium., 10.1016/s0015-0282(16)55823-3
  108. Redwine David B., Age-related evolution in color appearance of endometriosis**Presented at the annual meeting of districts VIII-IX of The American College of Obstetricians and Gynecologists, October 31, 1984, Scottsdale, Arizona, and at the forty-first annual clinical meeting of The American Fertility Society, September 28 to October 2, 1985, Chicago, Illinois., 10.1016/s0015-0282(16)59611-3
  109. Goldstein, J Reprod Med, 44, 251 (1980)
  110. Donnez Jacques, Lousse Jean-Christophe, Jadoul Pascale, Donnez Olivier, Squifflet Jean, Laparoscopic management of endometriomas using a combined technique of excisional (cystectomy) and ablative surgery, 10.1016/j.fertnstert.2009.02.065
  111. Brosens Ivo, The typical ovarian endometrioma has a surface origin, 10.1016/j.fertnstert.2010.07.1056
  112. Donnez Jacques, Reply of the Authors, 10.1016/j.fertnstert.2010.07.1057
  113. SAMPSON JOHN A., PERFORATING HEMORRHAGIC (CHOCOLATE) CYSTS OF THE OVARY : THEIR IMPORTANCE AND ESPECIALLY THEIR RELATION TO PELVIC ADENOMAS OF ENDOMETRIAL TYPE ("ADENOMYOMA" OF THE UTERUS, RECTOVAGINAL SEPTUM, SIGMOID, ETC.), 10.1001/archsurg.1921.01110080003001
  114. Hughesdon, J Obstet Gynaecol Br Emp, 44, 69 (1957)
  115. Brosens Ivo A., Puttemans Patrick J., Deprest Jan, The endoscopic localization of endometrial implants in the ovarian chocolate cyst, 10.1016/s0015-0282(16)56752-1
  116. Nezhat, J Reprod Med, 37, 771 (1992)
  117. Donnez J., Nisolle M., Gillet N., Smets M., Bassil S., Casanas-Roux F., Large ovarian endometriomas, 10.1093/humrep/11.3.641
  118. Serov, Histological Typing of Ovarian Tumors, 17 (1973)
  119. Motta, Submicrosc Cytol, 99, 664 (1992)
  120. Rosenfeld David L., Lecher B.Douglas, Endometriosis in a patient with Rokitansky-Kuster-Hauser syndrome, 10.1016/0002-9378(81)90418-x
  121. Canis, The Current Status of Endometriosis. Research and Management, 407 (1993)
  122. Donnez Jacques, CO2 laser laparoscopy in infertile women with endometriosis and women with adnexal adhesions, 10.1016/s0015-0282(16)59404-7
  123. Donnez, Woman's Health Today, 112 (1994)
  124. Nisolle, Endometriosis: Current Understanding and Management, 237 (1995)
  125. Hart, Cochrane Database Syst Rev, 16, CD004992 (2008)
  126. Beretta Paolo, Franchi Massimo, Ghezzi Fabio, Busacca Mauro, Zupi Errico, Bolis Pierfrancesco, Randomized clinical trial of two laparoscopic treatments of endometriomas: cystectomy versus drainage and coagulation, 10.1016/s0015-0282(98)00385-9
  127. Alborzi Saeed, Momtahan Mozhdeh, Parsanezhad Mohammad Ebrahim, Dehbashi Sedigheh, Zolghadri Jaleh, Alborzi Soroosh, A prospective, randomized study comparing laparoscopic ovarian cystectomy versus fenestration and coagulation in patients with endometriomas, 10.1016/j.fertnstert.2004.04.067
  128. Alborzi Saeed, Ravanbakhsh Romina, Parsanezhad Mohammad E., Alborzi Mehrnoosh, Alborzi Soroosh, Dehbashi Sedigheh, A comparison of follicular response of ovaries to ovulation induction after laparoscopic ovarian cystectomy or fenestration and coagulation versus normal ovaries in patients with endometrioma, 10.1016/j.fertnstert.2006.11.134
  129. Geber Selmo, Ferreira Daniela Parreiras, Prates Luis Felipe Víctor Spyer, Sales Liana, Sampaio Marcos, Effects of previous ovarian surgery for endometriosis on the outcome of assisted reproduction treatment, 10.1016/s1472-6483(10)61619-7
  130. Exacoustos Caterina, Zupi Errico, Amadio Annalisa, Szabolcs Beata, De Vivo Bonaventura, Marconi Daniela, Elisabetta Romanini Maria, Arduini Domenico, Laparoscopic removal of endometriomas: sonographic evaluation of residual functioning ovarian tissue, 10.1016/j.ajog.2004.01.010
  131. Somigliana E., Does laparoscopic excision of endometriotic ovarian cysts significantly affect ovarian reserve? Insights from IVF cycles, 10.1093/humrep/deg432
  132. Hachisuga T., Histopathological analysis of laparoscopically treated ovarian endometriotic cysts with special reference to loss of follicles, 10.1093/humrep/17.2.432
  133. Muzii Ludovico, Bellati Filippo, Bianchi Antonella, Palaia Innocenza, Manci Natalina, Zullo Marzio Angelo, Angioli Roberto, Panici Pierluigi Benedetti, Laparoscopic stripping of endometriomas: a randomized trial on different surgical techniques. Part II: pathological results, 10.1093/humrep/deh851
  134. SAMPSON JOHN A., INTESTINAL ADENOMAS OF ENDOMETRIAL TYPE : THEIR IMPORTANCE AND THEIR RELATION TO OVARIAN HEMATOMAS OF ENDOMETRIAL TYPE (PERFORATING HEMORRHAGIC CYSTS OF THE OVARY), 10.1001/archsurg.1922.01110140003001
  135. Donnez, An Atlas of Laser Operative Laparoscopy and Hysteroscopy, 83 (2001)
  136. Donnez J., Nisolle M., 10 Advanced laparoscopic surgery for the removal of rectovaginal septum endometriotic or adenomyotic nodules, 10.1016/s0950-3552(05)80398-0
  137. Donnez J., Nisolle M., Casanas-Roux F., Bassil S., Anaf V., Surgery: Rectovaginal septum, endometriosis or adenomyosis: laparoscopic management in a series of 231 patients, 10.1093/oxfordjournals.humrep.a136001
  138. Donnez Jacques, Nisolle Michelle, Gillerot Stephane, Smets Mireille, Bassil Salim, Casanas-Roux Francoise, Recto vaginal septum adenomyotic nodules: a series of 500 cases, 10.1111/j.1471-0528.1997.tb12059.x
  139. Donnez Jacques, Squifflet Jean, Laparoscopic excision of deep endometriosis, 10.1016/j.ogc.2004.06.006
  140. Donnez, Atlas of Operative Laparoscopy and Hysteroscopy, 63 (2007)
  141. Koninckx, Endometriosis: Current Understanding and Management, 264 (1995)
  142. Cornillie Freddy J., Oosterlynck Didier, Lauweryns Joseph M., Koninckx Philippe R., Deeply infiltrating pelvic endometriosis: histology and clinical significance, 10.1016/s0015-0282(16)53570-5
  143. Koninckx Philippe R., De Cicco Carlo, Schonman Ron, Corona Roberta, Betsas George, Ussia Anastasia, Letter to the Editor, 10.1016/j.jmig.2008.07.010
  144. Koninckx Philippe R., Martin Dan C., Deep endometriosis: a consequence of infiltration or retraction or possibly adenomyosis externa?**Supported by grant 9.0020.90 of the Belgian National Research Foundation (Nationale Loterij), Belgium., 10.1016/s0015-0282(16)55436-3
  145. Donnez Jacques, Donnez Olivier, Squifflet Jean, Nisolle Michelle, The concept of 'adenomyotic disease of the retroperitoneal space' is born, 10.1046/j.1365-2508.2001.00423.x
  146. Squifflet, Acta Gastro-enterol Belg, 67, 272 (2004)
  147. Chapron Charles, Chopin Nicolas, Borghese Bruno, Foulot Hervé, Dousset Bertrand, Vacher-Lavenu Marie Cécile, Vieira Marco, Hasan Wael, Bricou Alexandre, Deeply infiltrating endometriosis: pathogenetic implications of the anatomical distribution, 10.1093/humrep/del079
  148. Chapron Charles, Liaras Etienne, Fayet Patricia, Hoeffel Christine, Fauconnier Arnaud, Vieira Marco, Barakat Habib, Dousset Bertrand, Legmann Paul, Bonnin André, Dubuisson Jean-Bernard, Magnetic Resonance Imaging and Endometriosis: Deeply Infiltrating Endometriosis Does Not Originate from the Rectovaginal Septum, 10.1159/000064562
  149. Abrao M. S., Goncalves M. O. d. C., Dias J. A., Podgaec S., Chamie L. P., Blasbalg R., Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the diagnosis of deep endometriosis, 10.1093/humrep/dem187
  150. Donnez Jacques, Nisolle Michelle, Squifflet Jean, Ureteral endometriosis: a complication of rectovaginal endometriotic (adenomyotic) nodules, 10.1016/s0015-0282(01)02921-1
  151. Koninckx P.R., Braet P., Kennedy S.H., Barlow D.H., Dioxin pollution and endometriosis in Belgium, 10.1093/oxfordjournals.humrep.a138623
  152. van Kaam K.J.A.F., Schouten J.P., Nap A.W., Dunselman G.A.J., Groothuis P.G., Fibromuscular differentiation in deeply infiltrating endometriosis is a reaction of resident fibroblasts to the presence of ectopic endometrium, 10.1093/humrep/den153
  153. Van Langendonckt, Eur J Obstet Gynaecol Reprod Biol, 123, S35 (2005)
  154. Donnez J., Nisolle M., Casanas-Roux F., Brion P., DaFerreira N.C., Stereometric evaluation of peritoneal endometriosis and endometriotic nodules of the rectovaginal septum, 10.1093/oxfordjournals.humrep.a019024
  155. Anaf V., Simon P., El Nakadi I., Fayt I., Simonart T., Buxant F., Noel J-C., Hyperalgesia, nerve infiltration and nerve growth factor expression in deep adenomyotic nodules, peritoneal and ovarian endometriosis, 10.1093/humrep/17.7.1895
  156. Squifflet Jean, Feger Chantal, Donnez Jacques, Diagnosis and Imaging of Adenomyotic Disease of the Retroperitoneal Space, 10.1159/000066294
  157. Cullen, Johns Hopkins Hosp Rep, 133 (1896)
  158. Sampson John A., Ovarian Hematomas of Endometrial Type (Perforating Hemorrhagic Cysts of the Ovary) and Implantation Adenomas of Endometrial Type, 10.1056/nejm192204061861401
  159. Renish, Zeischr Geburtshilfe Gynaekol, 70, 585 (1912)
  160. Hudelist Gernot, Keckstein Joerg, Wright Jeremy T., The migrating adenomyoma: past views on the etiology of adenomyosis and endometriosis, 10.1016/j.fertnstert.2008.08.086
  161. Lockyer, Fibroids and Allied Tumours (Myoma and Adenomyoma) (1918)
  162. Vercellini Paolo, Frontino Giada, Pietropaolo Giuliana, Gattei Umberto, Daguati Raffaella, Crosignani Pier Giorgio, Deep Endometriosis: Definition, Pathogenesis, and Clinical Management, 10.1016/s1074-3804(05)60190-9
  163. Nakamura M., Katabuchi H., Tohya T., Fukumatsu Y., Matsuura K., Okamura H., Endometriosis: Scanning electron microscopic and immunohistochemical studies of pelvic endometriosis, 10.1093/oxfordjournals.humrep.a138006
  164. Kim M.R., Park D.W., Lee J.H., Choi D.S., Hwang K.J., Ryu H.S., Min C.K., Progesterone-dependent release of transforming growth factor-beta1 from epithelial cells enhances the endometrial decidualization by turning on the Smad signalling in stromal cells, 10.1093/molehr/gah240
  165. Haining R. E. B., Cameron I. T., van Papendorp C., Davenport A. P., Prentice A., Thomas E. J., Smith S. K., Epidermal growth factor in human endometrium: proliferative effects in culture and immunocytochemical localization in normal and endometriotic tissues, 10.1093/oxfordjournals.humrep.a137512
  166. Hirama Yoshiaki, Ochiai Kazunori, Estrogen and progesterone receptors of the out-of-phase endometrium in female infertile patients, 10.1016/s0015-0282(16)57534-7
  167. Laatikainen, Obstet Gynecol, 62, 592 (1983)
  168. Spirtos, Obstet Gynecol, 65, 535 (1985)
  169. Reich, J Reprod Med, 36, 516 (1991)
  170. Donnez, Laser Surgery, 148 (1991)
  171. 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, 10.1093/humrep/deq135
  172. Fleisch Markus C., Xafis Dimitris, Bruyne Filip De, Hucke Juergen, Bender Hans Georg, Dall Peter, Radical resection of invasive endometriosis with bowel or bladder involvement—Long-term results, 10.1016/j.ejogrb.2005.04.007
  173. CHAPRON CHARLES, CHOPIN NICOLAS, BORGHESE BRUNO, MALARTIC CECILE, DECUYPERE FOUZIA, FOULOT HERVE, Surgical Management of Deeply Infiltrating Endometriosis: An Update, 10.1196/annals.1335.035
  174. Emmanuel Kenneth R, Davis Colin, Outcomes and treatment options in rectovaginal endometriosis : , 10.1097/01.gco.0000175358.33555.ab
  175. Ford, JSLS, 9, 73 (2005)
  176. DARAI E, MARPEAU O, THOMASSIN I, DUBERNARD G, BARRANGER E, BAZOT M, Fertility after laparoscopic colorectal resection for endometriosis: preliminary results, 10.1016/j.fertnstert.2005.04.037
  177. Redwine David B., Wright Jeremy T., Laparoscopic treatment of complete obliteration of the cul-de-sac associated with endometriosis: long-term follow-up of en bloc resection, 10.1016/s0015-0282(01)01913-6
  178. Meuleman Christel, D'Hoore André, Van Cleynenbreugel Ben, Beks Nele, D'Hooghe Thomas, Outcome after multidisciplinary CO2 laser laparoscopic excision of deep infiltrating colorectal endometriosis, 10.1016/s1472-6483(10)60267-2
  179. Vercellini P., Crosignani P.G., Abbiati A., Somigliana E., Viganò P., Fedele L., The effect of surgery for symptomatic endometriosis: the other side of the story, 10.1093/humupd/dmn062
  180. Donnez, World Endometriosis Society e-journal, 10, 6 (2008)
  181. Fernandez H., Deffieux X., Faivre E., Gervaise A., Faut-il réellement opérer les lésions infiltrantes d’endométriose ? – Non « Choisir le réalisme et non l’idéalisme », 10.1016/j.gyobfe.2007.12.007
  182. Canis M., Matsuzaki S., Jardon K., Rivoire C., Cotte B., Tamburro S., Botchorishvili R., Rabischong B., Pouly J.-L., Mage G., Oui, il faut opérer les patientes qui ont des lésions d’endométriose infiltrante ! « Préférez l’optimisme de la volonté au pessimisme de l’intelligence ! », 10.1016/j.gyobfe.2007.12.008
Bibliographic reference Nisolle, Michelle ; Donnez, Jacques. Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities. In: Fertility and Sterility, Vol. 68, no. 4, p. 585-596 (1997)
Permanent URL http://hdl.handle.net/2078.1/24247