FRINK Linked Data Fragments server

Matches in SemOpenAlex for { <https://semopenalex.org/work/W2008360061> ?p ?o ?g. }

• W2008360061 endingPage "316" @default.
• W2008360061 startingPage "307" @default.
• W2008360061 abstract "To improve the still fragmented understanding of endometriosis, a life cycle approach was adopted that revealed unexpected aspects of the natural history of the disease throughout a woman's life. Three age-related stages of endometriosis are distinguished. In premenarcheal and adolescent endometriosis, 2 types can be distinguished: a classic form that can occur before menarche, and a congenital obstructive form that is caused by uterine anomaly and outflow obstruction. The lesions include superficial peritoneal implants, but adhesions and endometrioma can also occur. It is suggested that premenarcheal and possibly adolescent endometriosis develop by activation of resting stem cells shed at the time of neonatal retrograde uterine bleeding. In the adult, endometriosis can be related to uterine preconditioning by cyclic menstruations acting as a priming mechanism for deep placentation. In adult life, the typical lesions are peritoneal, ovarian, and deep or adenomyotic endometriosis. More recently, endometriosis has been associated with endometrial dysfunction and myometrial junctional zone hyperplasia. These uterine changes can be linked with some major obstetrical syndromes. In postmenopause, endometriosis can develop or be reactivated both in the presence or absence of exogenous estrogens and can spread to a variety of organs and structures causing constrictive lesions. To improve the still fragmented understanding of endometriosis, a life cycle approach was adopted that revealed unexpected aspects of the natural history of the disease throughout a woman's life. Three age-related stages of endometriosis are distinguished. In premenarcheal and adolescent endometriosis, 2 types can be distinguished: a classic form that can occur before menarche, and a congenital obstructive form that is caused by uterine anomaly and outflow obstruction. The lesions include superficial peritoneal implants, but adhesions and endometrioma can also occur. It is suggested that premenarcheal and possibly adolescent endometriosis develop by activation of resting stem cells shed at the time of neonatal retrograde uterine bleeding. In the adult, endometriosis can be related to uterine preconditioning by cyclic menstruations acting as a priming mechanism for deep placentation. In adult life, the typical lesions are peritoneal, ovarian, and deep or adenomyotic endometriosis. More recently, endometriosis has been associated with endometrial dysfunction and myometrial junctional zone hyperplasia. These uterine changes can be linked with some major obstetrical syndromes. In postmenopause, endometriosis can develop or be reactivated both in the presence or absence of exogenous estrogens and can spread to a variety of organs and structures causing constrictive lesions. Thomas Cullen was the first to describe, under the common name of “adenomyoma,” the full morphological and clinical picture of the conditions identified today as endometriosis and adenomyosis1Benagiano G. Brosens I. Who identified endometriosis?.Fertil Steril. 2011; 95: 13-16Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar; he defined adenomyoma as the presence of endometrial-like tissue in myometrial wall, rectovaginal septum, hilus of the ovary, uterine ligaments, rectal wall, and umbilicus.2Cullen T.S. The distribution of adenomyomata containing uterine mucosa.Arch Surg. 1921; 1: 215-228Crossref Google Scholar The name “endometriosis” was created by John A. Sampson3Sampson J.A. Perforating hemorrhagic (chocolate) cysts of the ovary.Arch Surg. 1921; 3: 245-323Crossref Google Scholar, 4Sampson J.A. Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity.Am J Obstet Gynecol. 1927; 14: 422-469Abstract Full Text PDF Google Scholar 7 years after his fundamental paper on ovarian endometriomas when, operating on women at the time of menstruation and observing bleeding of the lesions, he advanced the first theory on the pathogenesis, postulating that presence of lesions outside the uterus was due to tubal regurgitation and dissemination of eutopic endometrial cells. Peritoneal lesions became the signature of endometriosis and the introduction of laparoscopy in the 1960s added a golden tool for an accurate diagnosis and surgical treatment. As a result, endometriosis became a separate nosological entity vis-à-vis adenomyosis (and the uterus) and research became focused on how fragments of menstrual endometrium can implant on peritoneal surfaces and invade the underlying tissues.5Hill Jr., L.L. Aberrant endometrium.Am J Surg. 1932; 18: 303-321Abstract Full Text PDF Google Scholar Besides the classic theory, alternative mechanisms have been proposed, such as coelomic metaplasia,6Gruenwald P. Origin of endometriosis from the mesenchyme of the celomic walls.Am J Obstet Gynecol. 1942; 44: 470-474Abstract Full Text PDF Google Scholar transportation through veins or lymphatics,7Javert C.T. The spread of benign and malignant endometrium in the lymphatic system.Am J Obstet Gynecol. 1952; 64: 780-806PubMed Google Scholar the presence of embryonic vestiges,8Russell W.W. Aberrant portions of the mullerian duct found in an ovary.Am J Obstet Gynecol. 1979; 134: 225-226PubMed Google Scholar and more recently the transformation of bone marrow9Du H. Taylor H.S. Contribution of bone marrow–derived stem cells to endometrium and endometriosis.Stem Cells. 2007; 25: 2082-2086Crossref PubMed Scopus (164) Google Scholar and endometrial stem cells10Gargett C.E. Uterine stem cells: what is the evidence?.Hum Reprod Update. 2007; 13: 87-101Crossref PubMed Scopus (155) Google Scholar; but–to this day–menstrual regurgitation with the subsequent implantation of endometrial cells under facilitating circumstances still explains most ectopic localizations.11Nap A.W. Groothuis P.G. Demir A.Y. Evers J.L.H. Dunselman G.A.J. Pathogenesis of endometriosis.Best Pract Res Clin Obstet Gynaecol. 2004; 18: 233-244Abstract Full Text Full Text PDF PubMed Scopus (85) Google Scholar, 12Brosens I. Benagiano G. Endometriosis: a modern syndrome.Indian J Med Res. 2011; 133: 581-593PubMed Google Scholar During the last century, clinical interest and research have been largely focused on lesions and their direct consequences and endometriosis has been considered fundamentally a disease of the fertile period and more specifically of adulthood, while the significance of its presence in other periods of a woman's life has not received proper attention. Here, we wish to draw attention to the fact that understanding endometriosis (and to some extent also adenomyosis) requires a life cycle approach granting significance to its presence before menarche, during adolescence, in adulthood, and in postmenopause. Taking such an approach also means revisiting the specific impact of the uterus itself on the development of the condition during the various stages of life. The published literature was searched using Scopus and PubMed focusing on the terms “endometriosis,” “menarche,” “adolescence,” “reproduction,” “adult,” “adenomyosis,” and “menopause.” In addition, the references of major publications were included in the search. After this search we restricted further work on studies of endometriosis published in peer-reviewed gynecological journals reporting data in function of the different age groups. These were critically appraised and summarized. One point that should be stressed is the lack–to our knowledge–of epidemiological studies on adolescent or postmenopausal endometriosis. At best, there are relatively small series that can provide no basis for an epidemiological evaluation. Even in the case of adult disease, the lack of affordable, noninvasive diagnostic methods makes it impossible to evaluate its true incidence. Premenarcheal endometriosis occurs in the normal young girl before menarche and needs to be distinguished from a congenital obstructive form that appears after menarche and is caused by complete outflow obstruction in the menstruating young girl. Marsh and Laufer13Marsh E.E. Laufer M.R. Endometriosis in premenarcheal girls who do not have an associated obstructive anomaly.Fertil Steril. 2005; 83: 758-760Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar carefully documented a classic form of endometriosis in 5 premenarcheal girls aged between 8.5-13 years and with breast development from Tanner I-III having chronic pelvic pain for >6 months. In none of them could an obstructive abnormality of the reproductive tract be suspected. At laparoscopy, all 5 girls had clear and red lesions of peritoneal endometriosis. On biopsy the lesions included stroma (but no endometrial-like glands), vascular proliferation, hemosiderin deposits, macrophage proliferation, inflammation, ciliated epithelium, and/or adhesions (Table). In all of them the clinical situation improved substantially after surgical removal of the lesions. Because of a relapse of pelvic pain not responsive to hormonal therapy, in 2 girls–6 and 8 years later–a second-look laparoscopy was performed and the presence of endometriosis with glandular structures and stroma was confirmed by biopsy. Recently, more cases have been described of peritoneal endometriosis in a 9-year-old premenarcheal girl with cyclic pelvic pain since her 8th year of life14Ebert A.D. Fuhr N. David M. Schneppel L. Papadopoulos T. Histological confirmation of endometriosis in a 9-year-old girl suffering from unexplained cyclic pelvic pain since her eighth year of life.Gynecol Obstet Invest. 2009; 67: 158-161Crossref PubMed Scopus (18) Google Scholar and ovarian endometrioma in an 11-year-old premenarcheal girl15Gogacz M. Sarzyński M. Napierała R. Sierocińska-Sawa J. Semczuk A. Ovarian endometrioma in an 11-year-old girl before menarche: a case study with literature review.J Pediatr Adolesc Gynecol. 2012; 25: e5-e7Abstract Full Text Full Text PDF PubMed Scopus (8) Google Scholar and an 18-year-old woman.16Wright K.N. Laufer M.R. Endometriomas in adolescents.Fertil Steril. 2010; 94: 1529e7-1529e9Abstract Full Text Full Text PDF Scopus (9) Google ScholarTablePreferential localization and types of lesions of endometriosis according to age groupsAge groupLocalizationType of lesionsAdolescentPeritoneumAngiogenesis, subtleOvarian surfaceEndometriomaAdultPeritoneumTypical, adhesionsOvaryEndometriomaRectovaginal septumDeep adenomyomaPostmenopausalOvaryEndometriomaExtrapelvisObstructiveBrosens. Endometriosis: a life cycle approach? Am J Obstet Gynecol 2013. Open table in a new tab Brosens. Endometriosis: a life cycle approach? Am J Obstet Gynecol 2013. Adolescent endometriosis can occur in association with obstructive müllerian anomalies (eg, unicornuate uterus with rudimentary horn, or uterine didelphys with obstructed hemivagina, often present with pelvic pain secondary to hematometra or hematocolpos). The reported incidence in teenagers with genital tract anomalies varies between 11-40%.17Dovey S. Sanfilippo J. Endometriosis and the adolescent.Clin Obstet Gynecol. 2010; 53: 420-428Crossref PubMed Scopus (25) Google Scholar In 64 women with müllerian anomalies, the hypothesis was tested that the development of endometriosis depends upon the amount of retrograde menstruation and the ability of the immune response to remove the debris. Surgery confirmed the presence of endometriosis in 10 of 13 women with functioning endometrium, patent tubes, and outflow obstruction and in only 16 of 43 women with no obstruction (77% vs 37%, P < .01).18Olive D.L. Henderson D.Y. Endometriosis and müllerian anomalies.Obstet Gynecol. 1987; 69: 412-415PubMed Google Scholar An interesting case was a 12-year-old white girl with extensive unilateral endometriosis in association with uterus didelphys and unilateral wall fusion defect at laparoscopy; after correction of the vaginal obstruction a subsequent laparotomy showed no evidence of endometriosis.19Sanfilippo J.S. Wakim N.G. Schikler K.N. Yussman M.A. Endometriosis in association with uterine anomaly.Am J Obstet Gynecol. 1986; 154: 39-43Abstract PubMed Google Scholar Recently, Yang et al20Yang Y.P. Wang Y. Jie Yang J.Y. Wang S. Lang J.H. Adolescent endometriosis in China: a retrospective analysis of 63 cases.J Pediatr Adolesc Gynecol. 2012; 25: 295-299Abstract Full Text Full Text PDF PubMed Scopus (13) Google Scholar in 15 cases with a genital tract malformation noted a much earlier disease onset; in addition, the ovaries were involved in 14 of these girls. Traditionally, endometriosis has been thought to occur only rarely in adolescence, but an increasing awareness of the disease among the medical community, as well as the public, is making an early diagnosis more frequent.21Templeman C. Adolescent endometriosis.Obstet Gynecol Clin North Am. 2009; 36: 177-185Abstract Full Text Full Text PDF PubMed Scopus (15) Google Scholar Although its true incidence is difficult to quantify, estimates have been attempted; they vary among different studies between 19-73%.22Goldstein D.P. De Cholnoky C. Emansi S.J. Adolescent endometriosis.J Adolesc Health Care. 1980; 1: 37-41Abstract Full Text PDF PubMed Google Scholar, 23Davies G.D. Thillet E. Lindeman J. Clinical characteristics of adolescent endometriosis.J Adolesc Health. 1993; 14: 362-368Abstract Full Text PDF PubMed Google Scholar, 24Laufer M.R. Goitein L. Bush M. Cramer D.W. Emans S.J. Prevalence of endometriosis in adolescent girls with chronic pelvic pain not responding to conventional therapy.J Pediatr Adolesc Gynecol. 1997; 10: 199-202Abstract Full Text PDF PubMed Google Scholar, 25Reese K.A. Reddy S. Rock J.A. Endometriosis in an adolescent population: the Emory experience.J Pediatr Adolesc Gynecol. 1997; 9: 125-128Abstract Full Text PDF Google Scholar, 26Emmert C. Romann D. Riedel H.-H. Endometriosis diagnosed by laparoscopy in adolescent girls.Arch Gynecol Obstet. 1998; 261: 89-93Crossref PubMed Scopus (25) Google Scholar, 27Stavroulis A.I. Saridogan E. Creighton S.M. Cutner A.S. Laparoscopic treatment of endometriosis in teenagers.Eur J Obstet Gynecol Reprod Biol. 2006; 125: 248-250Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar Although a majority of women with endometriosis report symptoms starting in adolescence, diagnosis is often delayed in this patient population28Arruda M.S. Petta C.A. Abrao M.S. Benetti-Pinto C.L. Time elapsed from onset of symptoms of endometriosis in a cohort study of Brazilian women.Hum Reprod. 2003; 18: 756-759Crossref PubMed Scopus (140) Google Scholar and often the younger the women are at onset of symptoms, the longer the period before a diagnosis is posed.24Laufer M.R. Goitein L. Bush M. Cramer D.W. Emans S.J. Prevalence of endometriosis in adolescent girls with chronic pelvic pain not responding to conventional therapy.J Pediatr Adolesc Gynecol. 1997; 10: 199-202Abstract Full Text PDF PubMed Google Scholar Endometriosis occurs in approximately 70% of adolescent girls with chronic pelvic pain not responding to conventional medical therapy and the majority of patients have stage I29The American Fertility Society Revised American Fertility Society classification.Fertil Steril. 1985; 43: 351Abstract Full Text PDF PubMed Google Scholar disease.25Reese K.A. Reddy S. Rock J.A. Endometriosis in an adolescent population: the Emory experience.J Pediatr Adolesc Gynecol. 1997; 9: 125-128Abstract Full Text PDF Google Scholar The different appearances of peritoneal endometriosis are classified as early-active (red, glandular, or vesicular), advanced (black, puckered), and healed (white, fibrotic) implants (Figure 1 and Table).30Vasquez G. Cornillie F. Brosens I.A. Peritoneal endometriosis: scanning electron microscopy and histology of minimal pelvic endometriotic lesions.Fertil Steril. 1984; 42: 696-703Abstract Full Text PDF PubMed Google Scholar, 31Murphy A.A. Green W.R. Bobbie D. Unsuspected endometriosis documented by scanning electron microscopy in visually normal peritoneum.Fertil Steril. 1986; 46: 522-524Abstract Full Text PDF PubMed Google Scholar, 32Wiegerinck M.A.H.M. Van Dop P.A. Brosens I.A. The staging of peritoneal endometriosis by the type of active lesion in addition to the revised American Fertility Society classification.Fertil Steril. 1993; 60: 461-464Abstract Full Text PDF PubMed Google Scholar Visually, active peritoneal endometriosis shows intense angiogenesis that can be clearly observed during hydroflotation (Figure 2).33Brosens I. Gordts S. Campo R. Transvaginal hydrolaparoscopy but not standard laparoscopy reveals subtle endometriotic adhesions of the ovary.Fertil Steril. 2001; 75: 1009-1012Abstract Full Text Full Text PDF PubMed Scopus (45) Google Scholar, 34Laufer M.R. Sanfilippo J. Rose G. Adolescent endometriosis: diagnosis and treatment approaches.J Pediatr Adolesc Gynecol. 2003; 16: S3-11Abstract Full Text Full Text PDF PubMed Scopus (66) Google Scholar The anatomic distribution of peritoneal endometriosis supports Sampson's hypothesis of retrograde menstruation as the primary model of development of endometriosis.35Jenkins S. Olive D.L. Haney A.F. Endometriosis: pathogenetic implications of the anatomic distribution.Obstet Gynecol. 1986; 67: 335-338PubMed Google Scholar The clinical significance of these minor manifestations has remained controversial.36Jansen R.P.S. Minimal endometriosis and reduced fecundability: prospective evidence from an artificial insemination by donor program.Fertil Steril. 1986; 46: 141-143Abstract Full Text PDF PubMed Google Scholar, 37Jansen R.P.S. Russell P. Nonpigmented endometriosis: clinical, laparoscopic, and pathologic definition.Am J Obstet Gynecol. 1986; 155: 1154-1159Abstract PubMed Google Scholar In adolescence, most disease is atypical and transient, with subtle lesions suddenly emerging and then vanishing.38Stripling M.C. Martin D.C. Chatman D.L. Van der Zwaag R. Poston W.M. Subtle appearance of pelvic endometriosis.Fertil Steril. 1988; 49: 427-431Abstract Full Text PDF PubMed Google Scholar, 39Martin D.C. Hubert G.D. Van der Zwaag R. El-Zeky F.A. Laparoscopic appearances of peritoneal endometriosis.Fertil Steril. 1989; 51: 63-67Abstract Full Text PDF PubMed Google Scholar, 40Evers J.L.H. Land J.A. Dunselman G.A.J. Van Der Linden P.J.Q. Hamilton C.J.C.M. “The Flemish giant,” reflections on the defense against endometriosis, inspired by Professor Emeritus Ivo A. Brosens.Eur J Obstet Gynecol Reprod Biol. 1998; 81: 253-258Abstract Full Text Full Text PDF PubMed Scopus (7) Google Scholar, 41Kalu E. McAuley W. Richardson R. Teenagers, adolescents, endometriosis and recurrence: a retrospective analysis of recurrence following primary operative laparoscopy.Gynecol Surg. 2008; 5: 209-212Crossref Scopus (3) Google ScholarFigure 2Peritoneal angiogenesis (under hydroflotation)Show full captionVascular tangle of newly formed blood vessels surrounding peritoneal implants (top row), inside an endometrioma (middle row), and inside filmy adhesions (bottom row).Brosens. Endometriosis: a life cycle approach? Am J Obstet Gynecol 2013.View Large Image Figure ViewerDownload Hi-res image Download (PPT) Vascular tangle of newly formed blood vessels surrounding peritoneal implants (top row), inside an endometrioma (middle row), and inside filmy adhesions (bottom row). Brosens. Endometriosis: a life cycle approach? Am J Obstet Gynecol 2013. Commenting on the publication by Marsh and Laufer,13Marsh E.E. Laufer M.R. Endometriosis in premenarcheal girls who do not have an associated obstructive anomaly.Fertil Steril. 2005; 83: 758-760Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar the editor of Obstetrical and Gynecological Survey42Marsh E.E. Laufer M.R. Endometriosis in premenarcheal girls who do not have an associated obstructive anomaly.Obstet Gynecol Surv. 2005; 60: 517-519Crossref Scopus (1) Google Scholar speculated that the girls may have had antecedents to endometriosis rather than the classic form of the disorder and suggested that endometrial cells may be activated by a process of angiogenesis even long before menarche. While vascular endothelial growth factor (VEGF) expression produced by the endometrial cell varies with the phase of the menstrual cycle and is higher in the proliferative than in the secretory phase,43Shifren J.L. Tseng J.F. Zaloudek C.J. et al.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.J Clin Endocrinol Metab. 1996; 81: 3112-3118Crossref PubMed Scopus (531) Google Scholar the estrogenic effect of maternal steroids or the prepubertal estrogen secretion might be sufficient for stimulating angiogenesis in the neonatal implants to develop into early endometriosis. There is also the possibility that endometriosis may develop by mechanisms other than retrograde menstruation and implantation, such as coelomic metaplasia, embryonic müllerian rests, or even the persistence of the forms of embryonic endometriosis as recently described.44Signorile P.G. Baldi F. Bussani R. et al.Embryologic origin of endometriosis: analysis of 101 human female fetuses.J Cell Physiol. 2007; 227: 1653-1656Crossref Scopus (27) Google Scholar More generally, mesenchymal stem cells may be the principal source of endometriosis outside of the peritoneal cavity when they differentiate into endometrial cells in these locations.45Lin J. Xiang D. Zhang J.-L. Allickson J. Xiang C. Plasticity of human menstrual blood stem cells derived from the endometrium.J Zhejiang Univ Sci B. 2011; 12: 372-380Crossref PubMed Scopus (16) Google Scholar The study of endometrial stem cells has made great progress and their existence has now been confirmed through different approaches.46Figueira P.G.M. Abrão M.S. Krikun G. Taylor H. Stem cells in endometrium and their role in the pathogenesis of endometriosis.Ann N Y Acad Sci. 2011; 1221: 10-17Crossref PubMed Scopus (37) Google Scholar Since adult stem cells can reconstruct endometrial tissue in vivo,47Liu Z.-Z. Liu D. Xie J. Adult stem cells in the endometrium.Zhongguo Zuzhi Gongcheng Yanjiu (Chinese Journal of Tissue Engineering Research). 2012; 16: 5113-5117Google Scholar their possible involvement in the etiology of endometriosis has been suggested.48Gargett C.E. Ye L. Endometrial reconstruction from stem cells.Fertil Steril. 2012; 98: 11-20Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar Premenarcheal and even adolescent endometriosis may also develop from stem cells originating from retrograde neonatal uterine bleeding. The phenomenon of uterine bleeding in neonates has been described in detail in the German literature of the 1970s. Based on this phenomenon, the hypothesis can be formulated that, in rare cases, the estrogenic effect of maternal steroids, or the prepubertal estrogen secretion, might be sufficient to stimulate angiogenesis in endometrial cell clusters that may have attached themselves onto the peritoneum right after birth.49Oliveira F.R. Cruz C.D. del Puerto H.L. Vilamil Q.T.M.F. Reis F.M. Camargos A.F. Stem cells: are they the answer to the puzzling etiology of endometriosis?.Histol Histopathol. 2012; 27: 23-29PubMed Google Scholar A first study of 153 newborns found visible vaginal bleeding in 5.3% of the cases and occult bleeding, as shown by hemoglobin positive reaction, in 61.3%. Uterine bleeding usually began between days 4-7 of life and lasted a mean 3.2 days.50Kaiser R. Graessel G. Incidence and intensity of uterine bleeding in the neonate.Geburtshilfe Frauenheilkd. 1974; 34 ([in German]): 644-648PubMed Google Scholar A similar study of 350 newborn girls51Huber A. The frequency of physiologic vaginal bleeding of newborn infants.Zentralbl Gynakol. 1976; 98 ([in German]): 1017-1020PubMed Google Scholar revealed uterine bleeding during the week after birth in 25.4%, mostly demonstrable only by chemical micromethods, but also macroscopically visible in 3.3%. Histological and cytological controls confirmed these observations indicating that, as a rule, no menstrual withdrawal bleeding, but degenerative, regressional changes of endometrium occur leading to bleeding by diapedesis. Stem cells derived from the endometrium can today be obtained from women's menstrual blood45Lin J. Xiang D. Zhang J.-L. Allickson J. Xiang C. Plasticity of human menstrual blood stem cells derived from the endometrium.J Zhejiang Univ Sci B. 2011; 12: 372-380Crossref PubMed Scopus (16) Google Scholar, 46Figueira P.G.M. Abrão M.S. Krikun G. Taylor H. Stem cells in endometrium and their role in the pathogenesis of endometriosis.Ann N Y Acad Sci. 2011; 1221: 10-17Crossref PubMed Scopus (37) Google Scholar; they display stem cell markers and can differentiate into various cell types. They quickly regenerate after menstruation and secrete many growth factors displaying recurrent angiogenesis. Further studies should clarify whether premenarcheal and even adolescent endometriosis may originate from stem cells of retrograde neonatal uterine bleeding. Current knowledge of endometriosis is largely based on the inspection of endometriotic lesions in the abdominal cavity in women with infertility or pelvic pain. However, in recent years the picture has been expanded by molecular investigations of the eutopic endometrium and high-definition imaging of the uterus. Appearance of peritoneal endometriosis in the adult includes, in addition to peritoneal endometriosis, adenomyotic lesions or deep endometriosis and ovarian endometriomas52Nisolle M. Donnez J. Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities.Fertil Steril. 1998; 68: 585-596Abstract Full Text PDF Scopus (593) Google Scholar (Table). Deep endometriosis can be described as progressive endometriosis with smooth-muscle metaplasia. Clinicopathological studies indicate that, in contrast with superficial lesions, deep endometriosis is strongly associated with pelvic pain.53Cornillie F.J. Oosterlynck D. Lauweryns J.M. Koninckx P.R. Deeply infiltrating pelvic endometriosis: histology and clinical significance.Fertil Steril. 1990; 53: 978-983Abstract Full Text PDF PubMed Google Scholar, 54Koninckx P.R. Meuleman C. Demeyere S. Lesaffre E. Cornillie F.J. Suggestive evidence that pelvic endometriosis is a progressive disease, whereas deeply infiltrating endometriosis is associated with pelvic pain.Fertil Steril. 1991; 55: 759-765Abstract Full Text PDF PubMed Google Scholar, 55Koninckx P.R. Martin D.C. Deep endometriosis: a consequence of infiltration or retraction or possibly adenomyosis externa?.Fertil Steril. 1992; 58: 924-928Abstract Full Text PDF PubMed Google Scholar For many years the ovarian endometrioma has not been recognized as a form of endometriosis, until Hughesdon56Hughesdon P.E. The structure of endometrial cysts of the ovary.J Obstet Gynaecol Br Emp. 1957; 44: 481-487Crossref Google Scholar showed that, in contrast with luteal cysts, the ovarian endometrioma is in most cases a pseudocyst formed by invagination adherent to the posterior side of the parametrium as confirmed by ovarioscopy.57Brosens I.A. Puttemans P.J. Deprest J. The endoscopic localization of endometrial implants in the ovarian chocolate cyst.Fertil Steril. 1994; 61: 1034-1038Crossref PubMed Google Scholar A younger age seems to confer an increased risk of adverse pregnancy outcomes as manifested by lower birth weight, premature delivery, and small for gestational age that is independent of the major confounding sociodemographic factors.58Fraser A.M. Brockert J.E. Ward R.H. Association of young maternal age with adverse reproductive outcomes.N Engl J Med. 1995; 332: 1113-1117Crossref PubMed Scopus (519) Google Scholar This observation is consistent with the menstruation preconditioning hypothesis, which explains the decrease in the risk of adverse pregnancy outcome after adolescence and, in the absence of pregnancy, an increased risk of endometriosis. The number of peritoneal areas involved in endometriosis seems to increase in adolescence until the early twenties.59Redwine D.B. Age-related evolution in color appearance of endometriosis.Fertil Steril. 1987; 48: 1062-1063Abstract Full Text PDF PubMed Google Scholar Compared with our primate relatives, menstruation in human beings is not only extraordinarily heavy, but placentation is also exceptionally deep, with trophoblast invading not only the decidual endometrium but also the inner third of the myometrium, the uterine junctional zone (JZ) and its spiral arteries.60Brosens J.J. Pijnenborg R. Brosens I.A. The myometrial junctional zone spiral arteries in normal and abnormal pregnancies.Am J Obstet Gynecol. 2002; 187: 1416-1423Abstract Full Text Full Text PDF PubMed Scopus (286) Google Scholar According to the menstrual preconditioning hypothesis, cyclic endometrial remodeling and menstruation precondition the human uterus for pregnancy by creating tolerance to the injurious effects of a subsequent more severe insult.61Brosens J.J. Parker M.G. McIndoe A. Pijnenborg R. Brosens I.A. A role for menstruation in preconditioning the uterus for successful pregnancy.Am J Obstet Gynecol. 2009; 200: 615.e1-615.e6Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar The mechanisms underpinning preconditioning include reactive oxygen production, activation of redox-sensitive signaling pathways, expression of angiogenic factors such as VEGF, and resistance to apoptosis.62Otani H. Ischemic preconditioning: from molecular mechanisms to therapeutics.Antioxid Redox Signal. 2008; 10: 207-247Crossref PubMed Scopus (66) Google Scholar These factors are highly regulated in the endometrium in response to hormonal sig" @default.
• W2008360061 created "2016-06-24" @default.
• W2008360061 creator A5019225467 @default.
• W2008360061 creator A5053873727 @default.
• W2008360061 creator A5064297842 @default.
• W2008360061 date "2013-10-01" @default.
• W2008360061 modified "2023-09-23" @default.
• W2008360061 title "Endometriosis: a life cycle approach?" @default.
• W2008360061 cites W108658453 @default.
• W2008360061 cites W123512577 @default.
• W2008360061 cites W1502197914 @default.
• W2008360061 cites W1526062852 @default.
• W2008360061 cites W190587926 @default.
• W2008360061 cites W1925466818 @default.
• W2008360061 cites W1965074961 @default.
• W2008360061 cites W1967238686 @default.
• W2008360061 cites W1968557684 @default.
• W2008360061 cites W1969234722 @default.
• W2008360061 cites W1972389236 @default.
• W2008360061 cites W1973939452 @default.
• W2008360061 cites W1974993766 @default.
• W2008360061 cites W1976506071 @default.
• W2008360061 cites W1980087605 @default.
• W2008360061 cites W1984086036 @default.
• W2008360061 cites W1986118680 @default.
• W2008360061 cites W1986613211 @default.
• W2008360061 cites W1990024572 @default.
• W2008360061 cites W1991602702 @default.
• W2008360061 cites W1996903542 @default.
• W2008360061 cites W1997700356 @default.
• W2008360061 cites W2002098824 @default.
• W2008360061 cites W2002568617 @default.
• W2008360061 cites W2003398728 @default.
• W2008360061 cites W2006356335 @default.
• W2008360061 cites W2007623696 @default.
• W2008360061 cites W2007963957 @default.
• W2008360061 cites W2008065041 @default.
• W2008360061 cites W2010387940 @default.
• W2008360061 cites W2014463766 @default.
• W2008360061 cites W2017522870 @default.
• W2008360061 cites W2023317990 @default.
• W2008360061 cites W2027335812 @default.
• W2008360061 cites W2028030563 @default.
• W2008360061 cites W2029074042 @default.
• W2008360061 cites W2029261168 @default.
• W2008360061 cites W2033474074 @default.
• W2008360061 cites W2034492080 @default.
• W2008360061 cites W2039322698 @default.
• W2008360061 cites W2039605313 @default.
• W2008360061 cites W2041440843 @default.
• W2008360061 cites W2046380299 @default.
• W2008360061 cites W2052616147 @default.
• W2008360061 cites W2053649459 @default.
• W2008360061 cites W2054323092 @default.
• W2008360061 cites W2055943854 @default.
• W2008360061 cites W2058972914 @default.
• W2008360061 cites W2065053683 @default.
• W2008360061 cites W2066993395 @default.
• W2008360061 cites W2067509264 @default.
• W2008360061 cites W2071883174 @default.
• W2008360061 cites W2072944305 @default.
• W2008360061 cites W2073882976 @default.
• W2008360061 cites W2079497712 @default.
• W2008360061 cites W2084862726 @default.
• W2008360061 cites W2090807442 @default.
• W2008360061 cites W2091845445 @default.
• W2008360061 cites W2093790323 @default.
• W2008360061 cites W2096141938 @default.
• W2008360061 cites W2099844604 @default.
• W2008360061 cites W2100034137 @default.
• W2008360061 cites W2104675344 @default.
• W2008360061 cites W2109120076 @default.
• W2008360061 cites W2110234109 @default.
• W2008360061 cites W2111029287 @default.
• W2008360061 cites W2111297082 @default.
• W2008360061 cites W2111975495 @default.
• W2008360061 cites W2118366474 @default.
• W2008360061 cites W2119331560 @default.
• W2008360061 cites W2135112634 @default.
• W2008360061 cites W2136044953 @default.
• W2008360061 cites W2140246703 @default.
• W2008360061 cites W2140368652 @default.
• W2008360061 cites W2140590568 @default.
• W2008360061 cites W2144290102 @default.
• W2008360061 cites W2145213731 @default.
• W2008360061 cites W2146194938 @default.
• W2008360061 cites W2159678949 @default.
• W2008360061 cites W2163849184 @default.
• W2008360061 cites W2166646122 @default.
• W2008360061 cites W2168030046 @default.
• W2008360061 cites W2203749559 @default.
• W2008360061 cites W2210940027 @default.
• W2008360061 cites W2227993884 @default.
• W2008360061 cites W2269270215 @default.
• W2008360061 cites W2290029196 @default.
• W2008360061 cites W2291960606 @default.
• W2008360061 cites W2412295907 @default.
• W2008360061 cites W2413716016 @default.

• next