[en] 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.
Disciplines :
Reproductive medicine (gynecology, andrology, obstetrics)
Author, co-author :
NISOLLE, Michelle ; Centre Hospitalier Universitaire de Liège - CHU > Gynécologie-Obstétrique CHR
Donnez, Jacques
Language :
English
Title :
Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities
von Rokitansky C. Ueber Uterusdrusen-Neubildung in Uterus and Ovarialsarcomen (Uterine gland proliferation in uterine and ovarian sarcomas). Zeitschrift Gesellschaft für Aerzte zu Wien 1860;37:577.
Sampson JA. Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 1927;14:422-69.
Donnez J, Nisolle M, Casanas-Roux F, Grandjean P. Endometriosis: pathogenesis and pathophysiology. In: Shaw RW, editor. Endometriosis. Carnforth: Parthenon Publishing, 1990: 11-29.
Halme J, Hammond MG, Hulka JF, Raj S, Talbert LM. Retrograde menstruation in healthy women and in patients with endometriosis. Obstet Gynecol 1984;64:151-4.
Liu DTY, Hitchcock A. Endometriosis: its association with retrograde menstruation, dysmenorrhea and tubal pathology. Br J Obstet Gynaecol 1986;93:859-62.
Keettel WC, Stein RJ. The viability of the cast-off menstrual endometrium. Am J Obstet Gynecol 1951;61:440-2.
Kruitwagen RF, Poels LG, Willemsen WN, De Ronde IJ, Jap PH, Rolland R. Endometrial epithelial cells in peritoneal fluid during the early follicular phase. Fertil Steril 1991;55:297-303.
Te Linde RW, Scott RB. Experimental endometriosis. Am J Obstet Gynecol 1950;60:1147-73.
Scott RB, Te Linde RW, Wharton LR Jr. Further studies on experimental endometriosis. Am J Obstet Gynecol 1953; 66:1082-103.
Schenken RS, Asch RH, Williams RF, Hodgen GD. Etiology of infertility in monkeys with endometriosis: luteinized unruptured follicles, luteal phase defects, pelvic adhesions, and spontaneous abortions. Fertil Steril 1984;41:122-30.
Donnez J, Wayembergh M, Casanas-Roux F, Karaman Y, Willems T, Ferin J. Effect on ovulation of surgically induced endometriosis in rabbits. Gynecol Obstet Invest 1987;24: 131-7.
Foidart J-M, Béliard A, Donnez J. Endometriosis and invasion. In: Brosens I, Donnez J, editors. The current status of endometriosis research and management. Carnforth: Parthenon Publishing, 1993:35-9.
Béliard A, Donnez J, Nisolle M, Foidart J-M. Localization of laminin, fibronectin, E-cadherin, and integrins in endometrium and endometriosis. Fertil Steril 1997;67:266-72.
Lessey BA, Damjanovich L, Coutifaris C, Castelbaum A, Albelda SM, Buck CA. Integrin adhesion molecules in the human endometrium: correlation with the normal and abnormal menstrual cycle. J Clin Invest 1992;90:188-95.
Tabibzadeh S, Sun XZ. Cytokine expression in human endometrium throughout the menstrual cycle. Hum Reprod 1992; 7:1214-21.
Bridges JE, Prentice A, Roche W, Englefield P, Thomas EJ. Expression of integrin adhesion molecules in endometrium and endometriosis. Br J Obstet Gynaecol 1994;101:696-700.
Van der Linden PJ, De Goeij AF, Dunselman GA, Erkens HW, Evers JL. Expression of cadherins and integrins in human endometrium throughout the menstrual cycle. Fertil Steril 1995;63:1210-6.
Marbaix E, Kokorine I, Henriet P, Donnez J, Courtoy PJ, Eeckhout Y. The expression of interstitial collagenase in human endometrium is controlled by progesterone and by estradiol and is related to menstruation. Biochem J 1995;305: 1027-30.
Marbaix E, Kokorine I, Donnez J, Eeckhout Y, Courtoy P. Regulation and restricted expression of interstitial collagenase suggest a pivotal role in the initiation of menstruation. Hum Reprod 1996;11(2 Suppl):134-43.
Kokorine I, Marbaix E, Henriet P, Okada Y, Donnez J, Eeckhout Y, et al. Focal cellular origin and regulation of interstitial collagenase (matrix-metalloproteinase-1) are related to menstrual breakdown in the human endometrium. J Cell Sci 1996;109:2151-60.
Kokorine I, Nisolle M, Donnez J, Eeckhout Y, Courtoy PJ, Marbaix E. Expression of interstitial collagenase (matrix me-talloproteinase-1) is related to the activity of human endometriotic lesions. Fertil Steril 1997;68:246-51.
Spuijbroek MD, Dunselman GA, Menheere PP, Evers JL. Early endometriosis invades the extracellular matrix. Fertil Steril 1992;58:929-33.
Gaetje R, Kotzian S, Hermann G, Baumann R, Starzinski-Powitz A. Invasiveness of endometriotic cells in vitro. Lancet 1995;346:1463-4.
Jenkins S, Olive DL, Haney AF. Endometriosis: pathogenetic implications of the anatomic distribution. Obstet Gynecol 1986;67:335-8.
Ayers JW, Friedenstab AP. Utero-tubal hypotonia associated with pelvic endometriosis. The American Fertility Soc 1985; 131(supplement).
Bartosik D, Jacobs SL, Kelly LJ. Endometrial tissue in peritoneal fluid. Fertil Steril 1986;46:796-800.
Salamanca A, Beltran E. Subendometrial contractility in menstrual phase visualized by transvaginal sonography in patients with endometriosis. Fertil Steril 1995;64:193-5.
Cramer DW, Wilson E, Stillman RJ, Berger MJ, Belisle S, Schiff I, et al. The relation of endometriosis to menstrual characteristics, smoking, and exercise. J Am Med Assoc 1986; 255:1904-8.
Sanfilippo JS, Wakim NG, Schikler KN, Yussman MA. Endometriosis in association with uterine anomaly. Am J Obstet Gynecol 1986;154:39-43.
Simpson JL, Elias S. Malinak LR, Buttram VC. Heritable aspects of endometriosis. I. Genetic studies. Am J Obstet Gynecol 1980;137:327-31.
Steele RW, Dmowski WP, Marmer DJ. Immunologic aspects of human endometriosis. Am J Reprod Immunol 1984;6:33-6.
Oosterlynck D, Cornillie FJ, Waer M, Vandeputte M, Koninckx PR. Women with endometriosis show a defect in natural killer cell activity resulting in a decreased cytotoxicity to autologous endometrium. Fertil Steril 1991;56:45-51.
Dunselmann GA, Hendricx MG, Bouckaert PX, Evers JL. Functional aspects of peritoneal macrophages in endometriosis of women. J Reprod Fertil 1988;82:707-10.
Rana N, Braun DP, House R, Gebel H, Rotman C, Dmowski WP. Basal and stimulated secretion of cytokines by peritoneal macrophages in women with endometriosis. Fertil Steril 1996;65:925-30.
Koch AE, Polverini PJ, Kunkel SL, Harlow LA, Di Pietro LA, Einer VM, et al. Interleukin 8 as a macrophage derived mediator of angiogenesis. Science 1992;258:1798-801.
Zhang R, Wild R, Ojago J. Effect of tumor necrosis factor-α on adhesion of human endometrial cells to peritoneal mesothelial cells: an in vitro system. Fertil Steril 1993;59:1196-201.
Van der Linden PJ, de Goeij AF, Dunselman GA, Erkens HW, Evers JL. Endometrial cell adhesion in an in vitro model using intact amniotic membranes. Fertil Steril 1996;65:76-80.
Meyer R. Ueber den Stand der Frage der Adenomyositis und Adenomyome in Algemeinen und Insbesondere uéber Adenomyositis seroepithelialis und Adenomyometritis sacromatosa (The current question of adenomyositis and adenomyomas in general and particularly seroepithelial adenomyositis and sarcomatoid adenomyometritis). Zentralbl Gynakol 1919;43: 745-50.
Melicow MM, Pachter MR. Endometrial carcinoma of the prostatic utricle (uterus masculinus). Cancer 1967;20:1715-22.
Rosenfeld DL, Lecher BD. Endometriosis in a patient with Rokitansky-Kuster-Hauser syndrome. Am J Obstet Gynecol 1981;139:105-7.
Lauchlan SC. The secondary müllerian system. Obstet Gynecol Surv 1972;27:133-46.
Serov SF, Scully RE, Sobin LH. Histological typing of ovarian tumors. Geneva: World Health Organization, International histological classification of tumors. No. 9. 1973:17-21.
Fujii S. Secondary Müllerian system and endometriosis. Am J Obstet Gynecol 1991;162:219-25.
Nakamura M, Katabuchi H, Tohya TR, Fukumatsu Y, Matsuura K, Okamura H. Scanning electron microscopic and immunohistochemical studies of pelvic endometriosis. Hum Reprod 1993;8:2218-26.
Donnez J, Nisolle M, Casanas-Roux F, Brion P, Da Costa N. Stereometric evaluation of peritoneal endometriosis and endometriotic nodules of the rectovaginal septum. Hum Reprod 1995;11:224-8.
Nisolle M, Casanas-Roux F, Anaf V, Mine JM, Donnez J. Morphometric study of the stromal vascularization in peritoneal endometriosis. Fertil Steril 1993;59:681-4.
Nisolle M. Peritoneal, ovarian and rectovaginal endometriosis are three distinct entities [Thèse d'Agrégation de l'Enseignement Supérieur]. Louvain (Belgium): Université Catholique de Louvain, 1996.
Nisolle M, Donnez J, editors. Peritoneal, ovarian and rectovaginal endometriosis: the identification of three separate diseases. Carnforth: Parthenon Publishing, 1996.
Ferenczy A. Anatomy and histology of the uterine corpus. In: Kurman RJ, editor. Blaustein's pathology of the female genital tract. New York: Springer-Verlag, 1987:257-91.
Peek M, Landgren BM, Johannisson E. The endometrial capillaries during the normal menstrual cycle: a morphometric study. Hum Reprod 1992;7:906-11.
Nisolle M, Casanas-Roux F, Donnez J. Coexpression of cytokeratin and vimentin in eutopic endometrium and endometriosis throughout the menstrual cycle: evaluation by a computerized method. Fertil Steril 1995;64:69-75.
Nakopoulou L, Minaretzia D, Tsionou C, Mastrominas M. Value of immunohistochemical demonstration of several epithelial markers in hyperplasia and neoplastic endometrium. Gynecol Oncol 1990;37:346-53.
Norwitz ER, Fernandez-Shaw S, Barlow DH, Starkey PM. Expression of intermediate filament in endometrial glands changes with the onset of pregnancy and in endometriosis. Hum Reprod 1991;6:1470-3.
Bloom W, Fawcett DN. A textbook of histology. Philadelphia: WB Saunders, 1978:186-7.
Donnez J, Nisolle M. L'endométriose péritonéale, le kyste endométriotique ovarien et le nodule de la lame rectovaginale sont trois pathologies différentes [editorial]. Références en Gynécologie Obstétrique 1995;3:121-3.
Smith SK. Vascular endothelial growth factor and the endometrium. Hum Reprod 1996;11(2 Suppl):56-61.
Haining RE, Cameron IT, Van Pajendorps C, Davenport AP, Prentice A, Thomas EJ, et al. Epidermal growth factor in human endometrium: proliferative effects in culture and immunocytochemical localization in normal and endometriotic tissues. Hum Reprod 1991;6:1200-5.
Ferriani RA, Charnok-Jones DS, Prentice A, Thomas EJ, Smith SK. Immunohistochemical localization of acidic and basic fibroblast growth factors in normal human endometrium and endometriosis and the detection of their mRNA by polymerase chain reaction. Hum Reprod 1993;8:11-6.
Oosterlynck DJ, Meuleman C, Sobis H, Vandeputte M, Kon-inckx PR. Angiogenic activity of peritoneal fluid from women with endometriosis. Fertil Steril 1993;59:778-82.
Halme J, White C, Kauna S, Ester J, Haskill S. Peritoneal macrophages from patients with endometriosis release growth factor activity in vitro. J Clin Endocrinol Metab 1988; 66:1044-9.
Khorram O, Taylor RN, Ryan IP, Schall TJ, Landers DV. Peritoneal fluid concentrations of the cytokine RANTES correlate with the severity of endometriosis. Am J Obstet Gynecol 1993;169:1545-9.
Ryan IP, Tseng JF, Schriock ED, Khorram O, Landers DV, Taylor RN. Interleukin-8 concentrations are elevated in peritoneal fluid of women with endometriosis. Fertil Steril 1995; 63:929-32.
Brosens IA. Is mild endometriosis a disease? Is mild endometriosis a progressive disease? Hum Reprod 1994;9:2209-11.
Donnez J, Casanas-Roux F, Nisolle M. Peritoneal endometriosis: new histological aspects. In: Brosens IA, Donnez J, editors. The current status of endometriosis. Research and management. Carnforth: Parthenon Publishing, 1993:75-87.
Redwine DB. Age-related evolution in color appearance of endometriosis. Fertil Steril 1987;48:1062-3.
Goldstein MP, de Cholnoky C, Emans SJ, Leventhal JM. Laparoscopy in the diagnosis and management of pelvic pain in adolescents. J Reprod Med 1980;44:251-8.
Brosens IA, Koninckx PR, Corveleyn PA. A study of plasma progesterone, oestradiol-17 beta, prolactin and LH levels and of the luteal phase appearance of the ovaries in patients with endometriosis and infertility. Br J Obstet Gynaecol 1978;85: 246-50.
Bergqvist A, Ljunberg O, Myhre E. Human endometrium and endometriotic tissue obtained simultaneously: a comparative histologic study. Int J Gynecol Pathol 1984;3:135-45.
Mazur T, Kurman RJ. Normal endometrium and infertility evaluation. In: Mazur T, Kurman R, editors. Diagnosis of endometrial biopsies and curettings. A practical approach. New York: Springer-Verlag, 1995:7-32.
Bergqvist A, Ferno M. Estrogen and progesterone receptors in endometriotic tissue and endometrium: comparison of different cycle phases and ages. Hum Reprod 1993;8:2211-7.
Metzger DA. Cyclic changes in endometriosis implants. In: Brosens IA, Donnez J, editors. The current status of endometriosis. Research and management. Carnforth: Parthenon Publishing, 1993:89-108.
Nisolle M, Casanas-Roux F, Wyns CH, De Menten Y, Mathieu PE, Donnez J. Immunohistochemical analysis of estrogen and progesterone receptors in endometrium and peritoneal endometriosis: a new quantitative method. Fertil Steril 1994; 62:751-9.
Evers JL. The second-look laparoscopy for evaluation of the result of medical treatment of endometriosis should not be performed during ovarian suppression. Fertil Steril 1987; 47:502-4.
Sampson JA. Perforating haemorrhagic (chocolate) cysts of the ovary. Arch Surg 1921;3:245-323.
Hughesdon PE. The structure of endometrial cysts of the ovary. Journal of Obstetrics and Gynaecology British Empire 1957;44:69-84.
Brosens IA, Puttemans PJ, Deprest J. The endoscopic localization of endometrial implants in the ovarian chocolate cyst. Fertil Steril 1994;61:1034-8.
Nezhat F, Nezhat C, Allan CJ, Metzger DA, Sears DL. A clinical and histological classification of endometriomas: implications for a mechanism of pathogenesis. J Reprod Med 1992;37:771-6.
Donnez J, Nisolle M, Gillet N, Smets M, Bassil S, Casanas-Roux F. Large ovarian endometriomas. Hum Reprod 1996; 11:641-6.
Nisolle M, Donnez J. It is time to reassess the pathogenesis of ovarian endometriomas. Lancet (Submitted).
Motta PM, Van Blerkom J, Mekabe S. Changes in the surface morphology of ovarian germinal epithelium during the reproductive life and in some pathological conditions. Submicroscopy Cytology 1992;99:664-7.
Canis M, Wattiez A, Pouly JL, Bassil S, Bouquet J, Chapron C, et al. Laparoscopic treatment of endometriosis. In: Brosens IA, Donnez J, editors. The current status of endometriosis. Research and management. Carnforth: Parthenon Publishing, 1993:407-17.
Donnez J. CO2 laser laparoscopy in infertile women with endometriosis and women with adnexal adhesions. Fertil Steril 1987;48:390-4.
Donnez J, Nisolle M, Casanas-Roux F. Classification and endoscopic treatment of ovarian endometriosis. In: Popkin E, editor. Woman's health today. Carnforth: Parthenon Publishing, 1994:112-5.
Nisolle M, Donnez J. Conservative laparoscopic treatment of ovarian endometriosis. In: Shaw RW, editor. Endometriosis: current understanding and management. London: Blackwell Science Ltd, 1995:237-47.
Brosens IA, Van Ballaer P, Puttemans P, Deprest J. Reconstruction of the ovary containing large endometriomas by an extraovarian endosurgical technique. Fertil Steril 1996;66: 517-21.
Sampson JA. Intestinal adenomas of endometrial type. Arch Surg 1922;5:21-7.
Koninckx PR, Martin D. Deep endometriosis: a consequence of infiltration or retraction or possible adenomyosis externa? Fertil Steril 1992;58:924-8.
Donnez J, Nisolle M, Casanas-Roux F, Bassil S, Anaf V. Rectovaginal septum, endometriosis or adenomyosis: laparoscopic management in a series of 231 patients. Hum Reprod 1995;2:630-5.
Donnez J, Nisolle M, Smoes P, Gillet N, Beguin S, Casanas-Roux F. Peritoneal endometriosis and "endometriotic" nodules of the rectovaginal septum are two different entities. Fertil Steril 1996;66:362-8.
Reich H, McGlynn F, Salvat J. Laparoscopic treatment of cul-de-sac obliteration secondary to retrocervical deep fibrotic endometriosis. J Reprod Med 1991;36:516-22.
Zaloudek C, Norris HJ. Mesenchymal tumors of the uterus. In: Kurman R, editor. Blaustein's pathology of the female genital tract. New York: Springer-Verlag, 1987:373-408.
Scully RE, Richardson GS, Barlow JF. The development of malignancy in endometriosis. Clin Obstet Gynecol 1966;9: 384-411.
Scully RE. Sex cord-mesenzyme tumors: pathologic classification and its relation to prognosis and treatment. In: Junqeira AC, Gentile F, editors. Ovarian cancer. Heidelberg: Springer-Verlag, 1968, vol II, 40-56.
Hirama Y, Ochiai K. Estrogen and progesterone receptors of the out-of-phase endometrium in female infertile patients. Fertil Steril 1995;63:984-8.
Laatikainen T, Andersson B, Karkkainen J, Wahlström T. Progestin receptor levels in endometriomas with delayed or incomplete changes. Obstet Gynecol 1983;62:592-5.
Spirtos NY, Yurewicz EC, Moghissi KS, Magyar DM, Sundareson AS, Bottoms SF. Pseudocorpus luteum insufficiency: a study of cytosol progesterone receptors in human endometrium. Obstet Gynecol 1985;65:535-40.
Donnez J, Nisolle M, Smets M, Bassil S, Casanas-Roux F. Recto-vaginal septum adenomyotic nodule: a distinct entity. A series of 500 cases. Br J Obstet Gynaecol (in press).
