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• W1974879967 abstract "In this retrospective observational study involving 176 patients and 271 biopsies, the histologic differentiation in superficial endometriosis, deeply infiltrating endometriosis, and ovarian endometriomas was evaluated according to a previously proposed classification system. Results showed a predominance of the undifferentiated glandular pattern (33.5%) and mixed glandular pattern (46.9%) in deeply infiltrating endometriosis lesions, whereas the well-differentiated glandular pattern (41.8%) was most frequently seen in superficial endometriosis lesions, and in ovarian endometriomas a predominance of both the undifferentiated (40.5%) and mixed patterns (37.8%) was observed. In this retrospective observational study involving 176 patients and 271 biopsies, the histologic differentiation in superficial endometriosis, deeply infiltrating endometriosis, and ovarian endometriomas was evaluated according to a previously proposed classification system. Results showed a predominance of the undifferentiated glandular pattern (33.5%) and mixed glandular pattern (46.9%) in deeply infiltrating endometriosis lesions, whereas the well-differentiated glandular pattern (41.8%) was most frequently seen in superficial endometriosis lesions, and in ovarian endometriomas a predominance of both the undifferentiated (40.5%) and mixed patterns (37.8%) was observed. Endometriosis displays a broad spectrum of lesions, varying from mild to severely aggressive and disabling. Much of this aggressive behavior is related to the deep and infiltrative forms of the disease (1Abrão M.S. Neme R.M. Carvalho F.M. Adrighi J.M. Pinotti J.A. Histological classification of endometriosis as a predictor of response to treatment.Int J Gynaecol Obstet. 2003; 82: 31-40Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar). Deeply infiltrating endometriosis (DIE) is defined as the presence of lesions that penetrate 5 mm or more from the peritoneal surface (2Cornillie F.J. Osterlynck 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 Scopus (489) Google Scholar, 3Chapron C. Dubuisson J.B. Management of deep endometriosis.Ann N Y Acad Sci. 2001; 943: 276-280Crossref PubMed Scopus (42) Google Scholar) and occurs in 30%–40% of patients with endometriosis (4Yantiss R.K. Clement P.B. Young R.H. Endometriosis of the intestinal tract: a study of 44 cases of a disease that may cause diverse challenges in clinical and pathologic evaluation.Am J Surg Pathol. 2001; 25: 445-454Crossref PubMed Scopus (205) Google Scholar). A classification was proposed on the basis of the level of histologic tissue differentiation, suggesting that patients affected by endometriosis and having undifferentiated glands either in the pure or mixed form may require different therapeutic approaches (5Schweppe K.W. Wynn R.M. Endocrine dependency of endometriosis: an ultrastructural study. Eur J Obstet Gynecol Reprod Biol. 1984; 17: 193-208Abstract Full Text PDF PubMed Scopus (23) Google Scholar, 6Schweppe K.W. Wynn R.M. Ultrastructural changes in endometriotic implants during the menstrual cycle.Obstet Gynecol. 1981; 58: 465-473PubMed Google Scholar). In this study we sought to compare the histologic patterns of DIE, ovarian endometriosis (OE), and superficial endometriosis (SE) using the morphologic classification scheme previously described by Schweppe and Wynn (5Schweppe K.W. Wynn R.M. Endocrine dependency of endometriosis: an ultrastructural study. Eur J Obstet Gynecol Reprod Biol. 1984; 17: 193-208Abstract Full Text PDF PubMed Scopus (23) Google Scholar, 6Schweppe K.W. Wynn R.M. Ultrastructural changes in endometriotic implants during the menstrual cycle.Obstet Gynecol. 1981; 58: 465-473PubMed Google Scholar) and revisited by Abrao et al. (1Abrão M.S. Neme R.M. Carvalho F.M. Adrighi J.M. Pinotti J.A. Histological classification of endometriosis as a predictor of response to treatment.Int J Gynaecol Obstet. 2003; 82: 31-40Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar). We retrospectively analyzed 271 biopsies collected from 176 women between 2003 and 2006 at the Gynecologic Endoscopy and Endometriosis Clinic in the Obstetrics and Gynecology Department (Santa Casa de São Paulo Medical School). This study was approved by the local ethics and research board. All patient identification was kept confidential. Female patients of reproductive age with regular cycles and a histologically confirmed diagnosis of endometriosis were included. Women who had undergone antiestrogenic treatment in the last 3 months, or having malignant neoplasms diagnosed by routine tests, presence of other tubal or ovarian disease diagnosed at surgery, and clinical findings of premature ovarian failure were excluded. Patient ages ranged between 23 and 46 years, with a mean (± SD) age of 33.5 ± 5.4 years. Biopsies were divided into three groups according to depth and localization of lesions. Group I consisted of DIE lesions; this group was then subdivided according to the localization of lesion—uterosacral ligaments (right and left), bowel (rectosigmoid), and rectovaginal septum—for further analysis; group II was SE; and group III was OE. Biopsies were fixed in 10% formaldehyde and embedded in paraffin after routine processing in the Anatomic Pathology Clinic at Santa Casa de São Paulo Medical School. Histologic slices (4 mm thick) were stained with hematoxylin and eosin and visualized under light microscopy (Carl Zeiss, Jena, Germany). All specimens were simultaneously observed by two examiners (M.A.L.G. and G.K.). After histologic diagnosis of endometriosis we proceeded with morphologic classification of lesions, specifically focusing on ectopic endometrial structures (1Abrão M.S. Neme R.M. Carvalho F.M. Adrighi J.M. Pinotti J.A. Histological classification of endometriosis as a predictor of response to treatment.Int J Gynaecol Obstet. 2003; 82: 31-40Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar). Stromal endometriosis was defined as exclusive presence of stromal cells that are morphologically similar to the topic endometrium from any phase of the menstrual cycle (Fig. 1A ). If stromal cells were associated with glandular cells, we classified the lesion into one of the glandular patterns described below. Glandular endometriosis was defined as presence of superficial epithelium or an epithelium composed of glandular/cystic regions associated with signs of prior hemorrhage (presence of hemosiderophages and/or fibrosis). This pattern can be further subdivided according to its similarity to one of the following active endometrial epithelial forms: [1] well-differentiated glandular endometriosis (WDGE), in which ectopic epithelial cells are morphologically indistinguishable from those of the corresponding phases of the menstrual cycle (Fig. 1B); [2] undifferentiated glandular endometriosis (UGE), defined by flattened or low cuboidal epithelium having no similarity to the corresponding mesothelium of the peritoneal lining or any müllerian-type epithelium, distinct from endometrioid (Fig. 1C); and [3] mixed differentiated glandular endometriosis (MGE), defined as a population of differentiated and undifferentiated patterns localized within the same specimen (Fig. 1D). For qualitative variables, the absolute and relative frequencies of the lesions were calculated. Student's t-tests (7Rosner B. Fundamentals of biostatistics.2nd ed. PWS Publishers, Boston1986Google Scholar) were used for comparison of continuous variables, and χ2 or Fisher's exact tests were used for categoric variables. The Kolmogorov-Smirnov test was used to test the normality of data distribution. A significance level of 5% was established. The mean patient age was 33.13 ± 5.56 years in group I, 33.54 ± 5.39 years in group II, and 33.25 ± 5.33 in group III. No significant differences were observed among the three groups (P=.766). From 271 evaluated slides, 179 (66.05%) were of DIE lesions (group I), 55 (20.29%) of SE (group II), and 37 (13.65%) of OE (group III). In group I, 72 biopsies (30.8%) were collected from rectosigmoid nodules, 44 (18.8%) from the right uterosacral ligament, and 48 (20.5%) from the left uterosacral ligament. In 15 patients (6.4%), biopsies were collected from the rectovaginal septum. Prevalence of WDGE was higher in group II (41.8%) than in groups I (7.3%) and III (21.6%) (P<.001). Undifferentiated glandular endometriosis was more frequently observed in groups I (33.5%) and III (40.6%) compared with group II (12.7%) (P=.005). A pattern of MGE was found in 46.9% of group I lesions, 25.5% of group II, and 37.8% in group III (P=.016), whereas a stromal endometriosis pattern was seen in 12.3% of group I biopsies, 20% in group II, and in none of group III (P=.016, P=.1262 after partition analysis between groups I and II). When specifically focusing on DIE (group I), 72 of 179 total lesions were from rectosigmoidal nodules (40.2%), 92 from uterosacral ligaments (51.4%), and 15 from biopsies of the rectovaginal septum (8.4%). We observed a significantly higher percentage of the mixed glandular pattern in rectosigmoid biopsies (P=.014). When analyzing samples from the right and left uterosacral ligaments as well as from the rectovaginal septum, no significant difference was observed in the proportion of endometriosis with mixed-type histologic patterns (P=.666). Although endometriosis was previously described as a progressive and continuous disease (8Sampson J.A. Perforating hemorrhagic (chocolate) cysts of the ovary. Their importance and especially their relation to pelvic adenomas of the endometrial type (“adenomyoma” of the uterus, rectovaginal septum, sigmoid, etc.).Arch Surg. 1921; 3: 245-323Crossref Google Scholar), its etiology, pathophysiology, and natural history remain unknown (2Cornillie F.J. Osterlynck 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 Scopus (489) Google Scholar). Multiple studies have attempted to correlate disease stage with pain severity (9Fedele L. Parazzini F. Bianchi S. Arcaini L. Candiani G.B. Stage and localization of pelvic endometriosis and pain.Fertil Steril. 1990; 53: 155-158Abstract Full Text PDF PubMed Scopus (172) Google Scholar, 10Fedele L. Bianchi S. Bocciolone L. Di Nola G. Parazzini F. Pain symptons associated with endometriosis.Obstet Gynecol. 1992; 79: 767-769PubMed Google Scholar). Several authors believe that the term endometriosis is associated with more than one disease (11Garry R. The endometriosis syndromes: a clinical classification in the presence of aetiological confusion and therapeutic anarchy.Hum Reprod. 2004; 19: 760-768Crossref PubMed Scopus (60) Google Scholar, 12Nisolle M. Donnez J. Peritoneal endometriosis, ovarian endometriosis, and adenomyotic nodules of the rectovaginal septum are three different entities.Fertil Steril. 1997; 68: 585-596Abstract Full Text PDF PubMed Scopus (918) Google Scholar, 13Brosens I.A. Brosens J. Redefining endometriosis: a progressive disease.Hum Reprod. 2000; 15: 1-7Crossref PubMed Scopus (37) Google Scholar); it is therefore important to include histologic and morphometric parameters in addition to the traditional criteria used for diagnosing endometriosis. Various classification systems have been proposed to establish an efficient means of correlating histologic classification of endometriotic lesions with disease prognosis (14Hoeger K.M. Guzick D.S. Classification of endometriosis.Obstet Gynecol Clin North Am. 1997; 24: 347-359Abstract Full Text Full Text PDF PubMed Scopus (17) Google Scholar, 15Hoeger K.M. Guzick D.S. An update on the classification of endometriosis.Clin Obstet Gynecol. 1999; 42: 611-619Crossref PubMed Scopus (32) Google Scholar, 16Scurry J. Whitehead J. Healey M. Classification of ovarian endometriotic cysts.Int J Gynecol Pathol. 2001; 20: 147-154Crossref PubMed Scopus (25) Google Scholar); in this study, we sought to evaluate the correspondence between histologic differentiation and the degree of endometriotic infiltration. Schweppe and Wynn (5Schweppe K.W. Wynn R.M. Endocrine dependency of endometriosis: an ultrastructural study. Eur J Obstet Gynecol Reprod Biol. 1984; 17: 193-208Abstract Full Text PDF PubMed Scopus (23) Google Scholar) observed that poorly differentiated endometriotic foci did not respond to danazol treatment, whereas well-differentiated foci responded well, disappearing in 80% of the cases. Furthermore, danazol treatment on endometrial gland implants at various levels of differentiation (mixed differentiation) eliminated endometriosis or reverted proliferation rates to an earlier disease stage. They thus concluded that the ectopic endometrium differentially reacts to hormonal stimuli and that the response to danazol treatment decreases with a higher level of undifferentiation (5Schweppe K.W. Wynn R.M. Endocrine dependency of endometriosis: an ultrastructural study. Eur J Obstet Gynecol Reprod Biol. 1984; 17: 193-208Abstract Full Text PDF PubMed Scopus (23) Google Scholar). In the present study we found a predominance of mixed and undifferentiated endometriosis in DIE (group I) and OE (group III), as well as a predominance of cases with stromal and well-differentiated endometriosis in SE (group II). Because our patients have not undergone exogenous hormone treatment, we cannot directly correlate our results with those of Schweppe and Wynn (5Schweppe K.W. Wynn R.M. Endocrine dependency of endometriosis: an ultrastructural study. Eur J Obstet Gynecol Reprod Biol. 1984; 17: 193-208Abstract Full Text PDF PubMed Scopus (23) Google Scholar). However, our data suggest that undifferentiated endometriotic lesions are more invasive, possibly owing to the tissue's inability to respond to suppressor effects of the peritoneal fluid, which allows these endometrial foci to infiltrate more deeply. Another study (1Abrão M.S. Neme R.M. Carvalho F.M. Adrighi J.M. Pinotti J.A. Histological classification of endometriosis as a predictor of response to treatment.Int J Gynaecol Obstet. 2003; 82: 31-40Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar) found that undifferentiated endometriotic foci are more frequently associated with disease stages III and IV, as well as with rectovaginal localization. These investigators also found that complaints of pain decreased 5.71 times more in response to treatment with goserelin acetate and that the probability of future pregnancy was 2.57 times higher in women with well-differentiated endometriosis than in those with some degree of undifferentiated endometriosis (1Abrão M.S. Neme R.M. Carvalho F.M. Adrighi J.M. Pinotti J.A. Histological classification of endometriosis as a predictor of response to treatment.Int J Gynaecol Obstet. 2003; 82: 31-40Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar). These previous studies correlated histologic differentiation with lesion localization and treatment response, particularly for cases of superficial endometriosis. Our study suggests a possible histologic relationship among lesion localization, depth, and level of differentiation. Additionally, we found a significant prevalence of the more-differentiated pattern in superficial lesions compared with those in DIE and OE (1Abrão M.S. Neme R.M. Carvalho F.M. Adrighi J.M. Pinotti J.A. Histological classification of endometriosis as a predictor of response to treatment.Int J Gynaecol Obstet. 2003; 82: 31-40Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar, 6Schweppe K.W. Wynn R.M. Ultrastructural changes in endometriotic implants during the menstrual cycle.Obstet Gynecol. 1981; 58: 465-473PubMed Google Scholar). Given the higher frequencies of the undifferentiated glandular pattern in rectovaginal septal lesions, we sought to study the differentiation pattern according to localization of DIE nodules separately (1Abrão M.S. Neme R.M. Carvalho F.M. Adrighi J.M. Pinotti J.A. Histological classification of endometriosis as a predictor of response to treatment.Int J Gynaecol Obstet. 2003; 82: 31-40Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar). We therefore analyzed infiltrative endometriotic biopsies from the rectovaginal septum, uterosacral ligaments, and bowel (rectosigmoid nodules). All lesions were individually studied according to localization and histologic patterns previously described, and no significant differences were observed. We found a high prevalence of the mixed histologic group in all lesions examined. When specifically considering deep rectosigmoid endometriosis, our finding of a predominance of MGE contradicts that previously described in the literature, which found a predominance of UGE in cases of more aggressive endometriosis. Our findings in OE contradict those previously described in the literature. Specifically, a higher prevalence of WDGE in OE was reported, whereas we found a correlation with UGE in our study (1Abrão M.S. Neme R.M. Carvalho F.M. Adrighi J.M. Pinotti J.A. Histological classification of endometriosis as a predictor of response to treatment.Int J Gynaecol Obstet. 2003; 82: 31-40Abstract Full Text Full Text PDF PubMed Scopus (48) Google Scholar). One possible cause for this difference may be hormone oscillation in the ovarian environment, which leads to cyclic desquamation of the endometrial epithelium, cellular flattening, and changes in histologic patterns. Our histologic findings support the theory that endometriomas may be a part of the spectrum of DIE (11Garry R. The endometriosis syndromes: a clinical classification in the presence of aetiological confusion and therapeutic anarchy.Hum Reprod. 2004; 19: 760-768Crossref PubMed Scopus (60) Google Scholar), an association further supported by the increased probability of DIE in patients with OE (17Koninckx P.R. Barlow D. Kennedy S. Implantation versus infiltration: the Sampson versus the endometriotic disease theory.Gynecol Obstet Invest. 1999; 47(Suppl 1) (47Suppl): 3-10Crossref PubMed Scopus (60) Google Scholar). In the present study we observed a predominance of the well-differentiated pattern in more superficial lesions and the undifferentiated pattern in deeper lesions, suggesting a similar mechanism to explain the invasive potential of endometriosis. The detailed histologic classification scheme outlined in this study and in other studies can, it is hoped, be used as prognosis factors. Studies correlating histologic findings with patient evolution and response to clinical treatment, surgery, and relapse are urgently needed and may serve as the basis for more effective treatment guidelines in the near future. The authors thank Lia Mara Rossi for help with final manuscript composition and Creuza Dal Bó for statistical analysis." @default.
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• W1974879967 title "Histologic classification of specimens from women affected by superficial endometriosis, deeply infiltrating endometriosis, and ovarian endometriomas" @default.
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