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

Nisolle, Michelle; Donnez, Jacques

doi:10.1016/s0015-0282(97)00191-x

Cited by 1,279Endometriosis Research and TreatmentGynecological conditions and treatmentsEctopic Pregnancy Diagnosis and Management

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

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Nisolle, Michelle, Donnez, Jacques·1997·Fertility and Sterility

DOI 10.1016/s0015-0282(97)00191-x

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Abstract

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.

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On gross inspection, endometriosis is subdivided into superficial peritoneal endometriosis, deeply infiltrating endometriosis and ovarian cystic endometriosis.
“On gross inspection, endometriosis is subdivided into three categories: superficial peritoneal endometriosis, deeply infiltrating endometriosis (DIE) and ovarian (cystic) endometriosis (Brosens et al., 1993;Koninckx et al., 1994;Nisolle and Donnez, 1997; Table I).”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Nisolle and Donnez, 1997
Endometriosis is a common chronic inflammatory disease causing pain and infertility.
“endometriosis, a common chronic inflammatory disease causing pain and infertility [1,2,3]”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [2]
Estradiol has proinflammatory and antiapoptotic effects on endometrial cells, especially in ectopic foci.
“the impact of estradiol (E2), which is known to have proinflammatory and antiapoptotic effects on endometrial cells, especially in ectopic foci [2,3]”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [2]
Estrogens play a critical role in the pathogenesis of endometriosis.
“Biochemical, histological and clinical evidence show that estrogens play a critical role in the pathogenesis of endometriosis”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [2]
Dysmenorrhea and chronic non-menstrual pelvic pain are the most prevalent symptoms of endometriosis.
“although dysmenorrhea and chronic non-menstrual pelvic pain are the most prevalent [2]”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [2]

There are three distinct forms of endometriosis: peritoneal, ovarian and rectovaginal.
“There are three distinct forms of the disease (peritoneal, ovarian and rectovaginal endometriosis)”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [2]
Post-operative recurrence of endometriosis is common because persistent foci not detected at surgery may progress under the influence of circulating estrogens.
“post-operative recurrence is common, because persistent foci not detected at the time of surgery may progress under the influence of circulating estrogens [1,2,3,5,6].”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [2]
Endometriosis is clearly recognized as three separate entities since the original publication by Nisolle and Donnez in 1997.
“We would advocate a strategy based on the different phenotypes of endometriosis, clearly recognized as three separate entities since the original publication by Nisolle and Donnez in 1997 [2].”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [2]
DE is quite different from OE or PE and its histology resembles that of uterine adenomyosis.
“DE is quite different from OE or PE2 and its histology resembles that of uterine adenomyosis6.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [2]
Clinically, typical cystic and deep endometriosis lesions seem to be three different end points.
“Clinically, typical cystic and deep endometriosis lesions, thus seem to be three different end points as suggested previously (22,67).”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [22]

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Endometriosis
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Endometriosis
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Endometriosis: Epidemiology, Diagnosis and Clinical Management
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Vascular endothelial growth factor (VEGF) in endometriosis
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History of adenomyosis
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Pathophysiology of adenomyosis
Ferenczy, A. S. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.4.312 · Cited by 512 · see citing works
The Pathogenesis of Endometriosis: Molecular and Cell Biology Insights
Laganà, A. S., Garzon, S., Götte, M., Viganò, P., Franchi, M. P., Ghezzi, F., & Martin, D. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225615 · Cited by 492 · see citing works
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Stratton, P., & Berkley, K. J. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmq050 · Cited by 442 · see citing works
Oxidative stress and peritoneal endometriosis
Van Langendonckt, A., Casanas-Roux, F., & Donnez, J. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)02959-x · Cited by 391 · see citing works
Endometriosis
Brosens, I. A., & Brosens, J. J. (2000) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00265-7 · Cited by 392 · see citing works
Contemporary genetic technologies and female reproduction
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Pathogenesis of uterine adenomyosis, invagination or metaplasia?
García-Solares, J., Donnez, J., Donnez, O., & Dolmans, M.-M. (2018) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.12.030 · Cited by 339 · see citing works
Hyperalgesia, nerve infiltration and nerve growth factor expression in deep adenomyotic nodules, peritoneal and ovarian endometriosis
Anaf, V., Simon, P., El Nakadi, I., Fayt, I., Simonart, T., Buxant, F., & Noel, J.-C. (2002) · Human Reproduction · doi:10.1093/humrep/17.7.1895 · Cited by 317 · see citing works
The role of cytokines in endometriosis
Wu, M., & Ho, H. (2003) · American Journal of Reproductive Immunology · doi:10.1034/j.1600-0897.2003.01207.x · Cited by 317 · see citing works
Diagnostic accuracy of transvaginal sonography for deep pelvic endometriosis
Bazot, M., Thomassin‐Naggara, I., Hourani, R. G., Cortez, A., & Daraï, É. (2004) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.1108 · Cited by 318 · see citing works
The Main Theories on the Pathogenesis of Endometriosis
Lamceva, J., Uljanovs, R., & Strumfa, I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054254 · Cited by 324 · see citing works
Serum HE4 concentration differentiates malignant ovarian tumours from ovarian endometriotic cysts
Huhtinen, K., Suvitie, P. A., Hiissa, J., Junnila, J. J. T., Huvila, J. K., Kujari, H. P., Setälä, M., Härkki, P., Jalkanen, J. T., Fraser, J., et al. (2009) · British Journal of Cancer · doi:10.1038/sj.bjc.6605011 · Cited by 297 · see citing works
Extrapelvic Endometriosis: A Systematic Review
Andres, M. P., Arcoverde, F. V. L., Souza, C. C. C., Fernandes, L. F. C., Abrão, M. S., & Kho, R. M. (2020) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2019.10.004 · Cited by 276 · see citing works
Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules
Donnez, J., & Squifflet, J. (2010) · Human Reproduction · doi:10.1093/humrep/deq135 · Cited by 265 · see citing works
Endometriomas as a possible cause of reduced ovarian reserve in women with endometriosis
Kitajima, M., Defrère, S., Dolmans, M., Colette, S., Squifflet, J. P., Langendonckt, A. V., & Donnez, J. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.06.064 · Cited by 274 · see citing works
Functional MicroRNA Involved in Endometriosis
Hawkins, S. M., Creighton, C. J., Han, D. Y., Zariff, A., Anderson, M. L., Gunaratne, P. H., & Matzuk, M. M. (2011) · Molecular Endocrinology · doi:10.1210/me.2010-0371 · Cited by 264 · see citing works
Clinical Management of Endometriosis
Falcone, T., & Lebovic, D. I. (2011) · Obstetrics and Gynecology · doi:10.1097/aog.0b013e31822adfd1 · Cited by 263 · see citing works
Invasive and Noninvasive Methods for the Diagnosis of Endometriosis
Hsu, A. L., Khachikyan, I., & Stratton, P. (2010) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181db7ce8 · Cited by 260 · see citing works
Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity
Klemmt, P. A. B., Carver, J. G., Kennedy, S., Koninckx, P. R., & Mardon, H. J. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.08.046 · Cited by 256 · see citing works
Diagnosis of deep endometriosis: clinical examination, ultrasonography, magnetic resonance imaging, and other techniques
Bazot, M., & Daraï, É. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.10.026 · Cited by 253 · see citing works
Choosing the right surgical technique for deep endometriosis: shaving, disc excision, or bowel resection?
Donnez, O., & Roman, H. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.09.006 · Cited by 252 · see citing works
Oxidative stress in the pelvic cavity and its role in the pathogenesis of endometriosis
Donnez, J., Binda, M. M., Donnez, O., & Dolmans, M.-M. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.07.1075 · Cited by 251 · see citing works
Self-citation
Biomarkers in endometriosis: Challenges and opportunities
Ahn, S. H., Singh, V., & Tayade, C. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.01.009 · Cited by 242 · see citing works
Estrogen-progestins and progestins for the management of endometriosis
Vercellini, P., Buggio, L., Berlanda, N., Barbara, G., Somigliana, E., & Bosari, S. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.10.022 · Cited by 243 · see citing works
Pathogenesis of deep endometriosis
Gordts, S., Koninckx, P., & Brosens, I. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.08.036 · Cited by 241 · see citing works
High density of small nerve fibres in the functional layer of the endometrium in women with endometriosis
Tokushige, N., Markham, R., Russell, P., & Fraser, I. S. (2006) · Human Reproduction · doi:10.1093/humrep/dei368 · Cited by 236 · see citing works
Assessment of endometrial receptivity.
Lessey, B. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.07.1095 · Cited by 219 · see citing works
Reproductive performance, pain recurrence and disease relapse after conservative surgical treatment for endometriosis: the predictive value of the current classification system
Vercellini, P., Fedele, L., Aimi, G., Giorgi, O. D., Consonni, D., & Crosignani, P. G. (2006) · Human Reproduction · doi:10.1093/humrep/del230 · Cited by 232 · see citing works
Pathogenetic Mechanisms of Deep Infiltrating Endometriosis
Tosti, C., Pinzauti, S., Santulli, P., Chapron, C., & Petraglia, F. (2015) · Reproductive Sciences · doi:10.1177/1933719115592713 · Cited by 222 · see citing works
Laparoscopic management of endometriomas using a combined technique of excisional (cystectomy) and ablative surgery
Donnez, J., Lousse, J., Jadoul, P., Donnez, O., & Squifflet, J. P. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.02.065 · Cited by 218 · see citing works
Epithelial to mesenchymal transition-like and mesenchymal to epithelial transition-like processes might be involved in the pathogenesis of pelvic endometriosis†
Matsuzaki, S., & Darcha, C. (2012) · Human Reproduction · doi:10.1093/humrep/der442 · Cited by 216 · see citing works
Inflammation and nerve fiber interaction in endometriotic pain
McKinnon, B. D., Bertschi, D., Bersinger, N. A., & Mueller, M. D. (2014) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2014.10.003 · Cited by 214 · see citing works
The effect of surgical treatment for endometrioma on in vitro fertilization outcomes: a systematic review and meta-analysis
Tsoumpou, I., Kyrgiou, M., Gelbaya, T. A., & Nardo, L. G. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.05.049 · Cited by 212 · see citing works
The impact on ovarian reserve after laparoscopic ovarian cystectomy versus three-stage management in patients with endometriomas: a prospective randomized study
Tsolakidis, D., Pados, G., Vavilis, D., Athanatos, D., Tsalikis, T., Giannakou, A., & Tarlatzis, B. C. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.01.138 · Cited by 216 · see citing works
Platelets drive smooth muscle metaplasia and fibrogenesis in endometriosis through epithelial–mesenchymal transition and fibroblast-to-myofibroblast transdifferentiation
Zhang, Q., Duan, J., Liu, X., & Guo, S.-W. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.03.015 · Cited by 211 · see citing works
Transcriptional characterizations of differences between eutopic and ectopic endometrium
Wu, Y., Kajdacsy-Balla, A., Strawn, E., Basir, Z., Halverson, G., Jailwala, P., Wang, Y., Wang, X., Ghosh, S., & Guo, S.-W. (2006) · Endocrinology · doi:10.1210/en.2005-0426 · Cited by 208 · see citing works
Potential involvement of iron in the pathogenesis of peritoneal endometriosis
Defrere, S., Lousse, J. C., Gonzalez-Ramos, R., Colette, S., Donnez, J., & Van Langendonckt, A. (2008) · Molecular Human Reproduction · doi:10.1093/molehr/gan033 · Cited by 204 · see citing works
Histopathological analysis of laparoscopically treated ovarian endometriotic cysts with special reference to loss of follicles
Hachisuga, T. (2002) · Human Reproduction · doi:10.1093/humrep/17.2.432 · Cited by 201 · see citing works
Postoperative oral contraceptive exposure and risk of endometrioma recurrence
Vercellini, P., Somigliana, E., Daguati, R., Vigano, P., Meroni, F., & Crosignani, P. G. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.11.010 · Cited by 196 · see citing works
Endometriosis: A dysfunction and disease of the archimetra
Leyendecker, G. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.752 · Cited by 199 · see citing works
Genomewide Linkage Study in 1,176 Affected Sister Pair Families Identifies a Significant Susceptibility Locus for Endometriosis on Chromosome 10q26
Treloar, S. A., Wicks, J., Nyholt, D. R., Montgomery, G. W., Bahlo, M., Smith, V. E., Dawson, G., Mackay, I., Weeks, D. E., Bennett, S. T., et al. (2005) · The American Journal of Human Genetics · doi:10.1086/432960 · Cited by 195 · see citing works
Circulating MicroRNAs Identified in a Genome-Wide Serum MicroRNA Expression Analysis as Noninvasive Biomarkers for Endometriosis
Wang, W.-T., Zhao, Y.-N., Han, B.-W., Hong, S.-J., & Chen, Y.-Q. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2415 · Cited by 193 · see citing works
Kinase signalling pathways in endometriosis: potential targets for non-hormonal therapeutics
McKinnon, B. D., Kocbek, V., Nirgianakis, K., Bersinger, N. A., & Mueller, M. D. (2016) · Human Reproduction Update · doi:10.1093/humupd/dmv060 · Cited by 194 · see citing works
Evaluation of a panel of 28 biomarkers for the non-invasive diagnosis of endometriosis
Vodolazkaia, A., El-Aalamat, Y., Popovic, D., Mihalyi, A., Bossuyt, X., Kyama, C. M., Fassbender, A., Bokor, A., Schols, D., Huskens, D., et al. (2012) · Human Reproduction · doi:10.1093/humrep/des234 · Cited by 189 · see citing works
Strengths and limitations of diagnostic tools for endometriosis and relevance in diagnostic test accuracy research
Pascoal, E., Wessels, J. M., Aas‐Eng, M. K., Abrão, M. S., Condous, G. S., Jurkovic, D., Espada, M., Exacoustós, C., Ferrero, S., Guerriero, S., et al. (2022) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.24892 · Cited by 204 · see citing works
Smooth muscles are frequent components of endometriotic lesions
Anaf, V. (2000) · Human Reproduction · doi:10.1093/humrep/15.4.767 · Cited by 183 · see citing works
The role of TGF-β in the pathophysiology of peritoneal endometriosis
Young, V. J., Ahmad, S. F., Duncan, W. C., & Horne, A. W. (2017) · Human Reproduction Update · doi:10.1093/humupd/dmx016 · Cited by 188 · see citing works
Vascular development in endometriosis
Groothuis, P. G., Nap, A. W., Winterhager, E., & Grümmer, R. (2005) · Angiogenesis · doi:10.1007/s10456-005-9005-x · Cited by 183 · see citing works
An international terminology for endometriosis, 2021,
International Working Group of AAGL, E., Tomassetti, C., JOHNSON, N. P., Petrozza, J. C., Abrão, M. S., Einarsson, J. I., Horne, A. W., Lee, T. T. M., Missmer, S. A., Vermeulen, N., et al. (2021) · Human Reproduction Open · doi:10.1093/hropen/hoab029 · Cited by 182 · see citing works
Involvement of the nuclear factor-κB pathway in the pathogenesis of endometriosis
González-Ramos, R., Van Langendonckt, A., Defrère, S., Lousse, J.-C., Colette, S., Devoto, L., & Donnez, J. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.01.013 · Cited by 179 · see citing works
Deep Endometriosis: Definition, Pathogenesis, and Clinical Management
Vercellini, P., Frontino, G., Pietropaolo, G., Gattei, U., Daguati, R., & Crosignani, P. G. (2004) · The Journal of the American Association of Gynecologic Laparoscopists · doi:10.1016/s1074-3804(05)60190-9 · Cited by 180 · see citing works
Transvaginal sonography and rectal endoscopic sonography for the assessment of pelvic endometriosis: a preliminary comparison
Bazot, M. (2003) · Human Reproduction · doi:10.1093/humrep/deg314 · Cited by 179 · see citing works
Reduction of apoptosis and proliferation in endometriosis
Béliard, A., Noël, A., & Foidart, J. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.11.048 · Cited by 179 · see citing works
Structural abnormalities of the uterine wall in women with endometriosis and infertility visualized by vaginal sonography and magnetic resonance imaging
Kunz, G., Beil, D., Huppert, P., & Leyendecker, G. (2000) · Human Reproduction · doi:10.1093/humrep/15.1.76 · Cited by 177 · see citing works
Ovarian surgery for bilateral endometriomas influences age at menopause
Coccia, M. E., Rizzello, F., Mariani, G., Bulletti, C., Palagiano, A., & Scarselli, G. F. (2011) · Human Reproduction · doi:10.1093/humrep/der286 · Cited by 177 · see citing works
Endometriosis: A Disease That Remains Enigmatic
Acién, P., & Velasco, I. (2013) · ISRN Obstetrics and Gynecology · doi:10.1155/2013/242149 · Cited by 182 · see citing works
Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review
Donnez, J., & Dolmans, M.-M. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10051085 · Cited by 182 · see citing works
Bladder endometriosis must be considered as bladder adenomyosis
Donnez, J., Spada, F., Squifflet, J. P., & Nisolle, M. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01584-3 · Cited by 176 · see citing works
Ureteral endometriosis: a complication of rectovaginal endometriotic (adenomyotic) nodules
Donnez, J., Nisolle, M., & Squifflet, J. P. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(01)02921-1 · Cited by 175 · see citing works
Ovarian response during IVF–embryo transfer cycles after laparoscopic ovarian cystectomy for endometriotic cysts of >3 cm in diameter
Canis, M. J., Pouly, J. L., Tamburro, S., Mage, G., Wattiez, A., & Bruhat, M. A. (2001) · Human Reproduction · doi:10.1093/humrep/16.12.2583 · Cited by 174 · see citing works
Molecular and Cellular Pathogenesis of Endometriosis
Klemmt, P. A. B., & Starzinski‐Powitz, A. (2017) · Current Women s Health Reviews · doi:10.2174/1573404813666170306163448 · Cited by 175 · see citing works
Ovarian response after laparoscopic ovarian cystectomy for endometriotic cysts in 132 monitored cycles
Loh, F.-H., Tan, A. T., Kumar, J., & Ng, S.-C. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00207-1 · Cited by 172 · see citing works
Medical and surgical management of adenomyosis
Farquhar, C. M., & Brosens, I. A. (2006) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2006.01.012 · Cited by 171 · see citing works
Epithelial-to-mesenchymal transition in the development of endometriosis
Yang, Y., & Yang, W. (2017) · Oncotarget · doi:10.18632/oncotarget.16472 · Cited by 167 · see citing works
Recommendations for the surgical treatment of endometriosis. Part 2: deep endometriosis †‡¶
Working group of ESGE, E., Keckstein, J., Becker, C. M., Canis, M. J., Féki, A., Grimbizis, G., Hummelshøj, L., Nisolle, M., Roman, H., Sarıdoğan, E., et al. (2020) · Human Reproduction Open · doi:10.1093/hropen/hoaa002 · Cited by 170 · see citing works
Accuracy of magnetic resonance imaging and rectal endoscopic sonography for the prediction of location of deep pelvic endometriosis
Bazot, M., Bornier, C., Dubernard, G., Roseau, G., Cortez, A., & Daraï, E. (2007) · Human Reproduction · doi:10.1093/humrep/dem008 · Cited by 160 · see citing works
Progesterone receptor ligands for the treatment of endometriosis: the mechanisms behind therapeutic success and failure
Reis, F. M., Coutinho, L. M., Vannuccini, S., Batteux, F., Chapron, C., & Petraglia, F. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa009 · Cited by 166 · see citing works
MicroRNA expression profile in endometriosis: its relation to angiogenesis and fibrinolytic factors
Braza-Boïls, A., Marí-Alexandre, J., Gilabert, J., Sánchez-Izquierdo, D., España, F., Estellés, A., & Gilabert-Estellés, J. (2014) · Human Reproduction · doi:10.1093/humrep/deu019 · Cited by 164 · see citing works
Recent insights on the genetics and epigenetics of endometriosis
Borghese, B., Zondervan, K. T., Abrão, M. S., Chapron, C., & Vaiman, D. (2016) · Clinical Genetics · doi:10.1111/cge.12897 · Cited by 162 · see citing works
Role of laparoscopic treatment of endometriosis in patients with failed in vitro fertilization cycles
Littman, E. D., Giudice, L. C., Lathi, R. B., Berker, B., Milki, A. A., & NEZHAT, C. R. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.02.059 · Cited by 162 · see citing works
Does ovarian surgery for endometriomas impair the ovarian response to gonadotropin?
Donnez, J., Wyns, C., & Nisolle, M. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)02011-8 · Cited by 162 · see citing works
The impact of laparoscopic cystectomy on ovarian reserve in patients with unilateral and bilateral endometriomas
Alborzi, S., Keramati, P., Younesi, M., Samsami, A., & Dadras, N. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.10.019 · Cited by 158 · see citing works
Retracted
Endometrial and peritoneal expression of aromatase, cytokines, and adhesion factors in women with endometriosis
Kyama, C. M., Overbergh, L., Mihalyi, A., Meuleman, C., Mwenda, J. M., Mathieu, C., & D’Hooghe, T. M. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.02.057 · Cited by 157 · see citing works
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Nuclear factor-kappa B is constitutively activated in peritoneal endometriosis
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Peritoneal endometriosis, ovarian endometriosis and adenomyotic nodules of the rectovaginal septum: a different histopathogenesis?
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Peritoneal, ovarian and recto-vaginal endometriosis are three distinct entities
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Peritoneal endometriosis and “endometriotic” nodules of the rectovaginal septum are two different entities
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Reprint of: Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities
Nisolle, M., & Donnez, J. (2019) · Fertility and Sterility · doi:10.1016/j.fertnstert.2019.08.081 · Cited by 33 · see citing works

Authors: Nisolle, M., & Donnez, J.
Affiliations: Cliniques Universitaires Saint-Luc (BE)
ORCID: Nisolle, Michelle
Venue: Fertility and Sterility
Publisher: Elsevier BV
Published: 1997-10
Volume: 68
Issue: 4
Pages: 585-596
ISSN: 0015-0282 (ISSN-L)
DOI: 10.1016/s0015-0282(97)00191-x
OpenAlex: W2118366474
Cited by: 1,279
References: 96
Citations by year: 2026: 32 · 2025: 49 · 2024: 50 · 2023: 62 · 2022: 74 · 2021: 67 · 2020: 84 · 2019: 51 · 2018: 54 · 2017: 66 · 2016: 39 · 2015: 38 · 2014: 48 · 2013: 40 · 2012: 44
FWCI: 4.73
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 9112 d)
Locations: Fertility and Sterility (publishedVersion)
PubMed (publishedVersion)
Open Repository and Bibliography (University of Liège) (submittedVersion)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
Keywords: peritoneal endometriosis, endometrioma, adenomyoma, endometriosis pathogenesis, histogenesis, metaplasia, Müllerian origin, immunocytochemistry, infertility, pelvic pain
MeSH terms: Endometriosis, Female, Humans, Ovarian Diseases, Peritoneal Diseases, Rectal Diseases, Vaginal Diseases

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

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