CoChat
Sign Up
Cited by 69Endometriosis Research and TreatmentEctopic Pregnancy Diagnosis and ManagementGynecological conditions and treatments

Redefining endometriosis: is deep endometriosis a progressive disease?

Brosens, I.A., Brosens, J.J.·2000·Human Reproduction
DOI 10.1093/humrep/15.1.1
Open this paper in CoChat — free account

Abstract

Current literature on endometriosis distinguishes between superficial and deep lesions. Deep lesions are assumed to reflect invasive and progressive disease. The American Fertility Society classification system for endometriosis (American Fertility Society, 1985) distinguishes lesions, which extend below the surface of the peritoneum and the ovaries by <1, 1–3 and >3 cm and scores them 2–8 times higher than superficial lesions. More recently, some authors have recommended to make a distinction at 6 mm, suggesting that lesions deeper than 5 mm represent progressive disease (Cornillie et al., 1990). The concept of deep, and therefore progressive disease is based on Sampson's hypothesis that endometriosis is due to the menstrual dissemination into the peritoneal cavity (Sampson, 1927). Although this view may appear logical, there is little evidence that superficial endometriosis progresses to deep endometriosis. Before Sampson the localizations of ectopic endometrial-like tissue were described (Cullen, 1920) to occur principally along the Müllerian tract, including the inner third of the myometrium (adenomyosis), the posterior fornix and the uterine ligaments. All these lesions were described as adenomyotic nodules. On the other hand, Sampson (1921) discovered endometriosis by observing menstrual shedding in endometrial-like tissue lining the wall of chocolate cysts of the ovary (Sampson, 1921). When Sampson's reflux concept became generally accepted, all ectopic, endometrial-like tissue outside the uterus became endometriosis and as a consequence the confusing terminology of deep endometriosis was introduced. In this debate we will try to demonstrate that the classification of endometriosis should not be based on depth, but on the expression of a specific endometrial activity: sex steroid hormone-dependent bleeding or smooth muscle metaplasia. Tabibzadeh et al. performed elegant in-vitro studies to address the mechanisms underlying the spatial polarization of the eutopic endometrium into the basal and superficial layers (Tabibzadeh et al., 1993). They demonstrated that the `classical' sex steroid hormone (SSH)-dependent differentiation of endometrial cells can be abrogated by factors, e.g. interferon-γ which are released in the eutopic endometrium by resident CD3-positive T-lymphocyte aggregates in the endometrio–myometrial junction. The absence of a `classical' SSH-dependent differentiation process in the basal layer does not imply cellular refractoriness to ovarian hormones. The basal endometrial layer is the site of active cyclic metaplasia of the basal endometrial stromal cells into myofibroblasts and vice versa (Fujii et al., 1989) and a source of factors, e.g. endothelins and prostaglandins, that modulate the response of underlying junctional zone myometrium to ovarian hormones (Bacon et al., 1995). Evidence for metaplasia can be found in the endometrium, e.g. decidual stromal cells express α-smooth muscle actin and show ultrastructural similarities with myofibroblasts (Oliver et al., 1999). In summary, the morphological endometrial activity is manifested in the superficial layer by predecidualization and menstrual bleeding and in the basal layer/junctional zone compartment by cyclic smooth muscle metaplasia and differentiation. Active ectopic endometrial-like tissue is also morphologically characterized by either cyclic bleeding and endometrioma formation or smooth mucle metaplasia and fibromuscular nodule formation. In peritoneal and ovarian endometriosis the endometrial activity is characterized by menstrual shedding or SSH-dependent bleeding, as originally observed and described (Sampson, 1921). Peritoneal lesions are most active when they are superficial and haemorrhagic and become less active when they heal by fibrosis to become deeper and form fibrotic nodules (Nisolle and Donnez, 1997). The typical ovarian endometrioma is an even more striking example of superficial endometrial activity. Detailed histopathological studies have been based on ovaries with the chocolate cyst in situ. Sampson (1921) showed on such specimens that foci of endometrial-like tissue are lining the wall and manifesting menstrual shedding. Hughesdon (1957) found no evidence that `ectopic endometrium ate its way into the ovary like insects eating into an apple'. On resected specimens the endometrial tissue can appear deep due to tangential section, dislocation or, as documented in detail on an in-situ specimen by Sampson (1921), by early colonization of a lutein cyst at the site of communication with a small endometrioma. Our endoscopic investigations of large in-situ endometriomata, complemented by selective biopsies, have shown that in young women where fibrosis is absent, the endometrial lining is patchily distributed and loosely attached to the white ovarian cortex (Brosens et al., 1994). These observations have led to the hypothesis that the chocolate cyst is secondary to an endometriotic bleeding involving adhesions a

Integrity signals

Registry

Crossref · 10.1093/humrep/15.1.1

Cites

38 of 38 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The first phenotype characterized by poor sex steroid hormone response is along the Müllerian tract including the uterus, rectovaginal septum, and, to some extent, the uterine ligaments, and the second phenotype outside the Müllerian tract particularly the ovaries.

    “The first phenotype characterized by poor sex steroid hormone response is along the M€ ullerian tract including the uterus, rectovaginal septum, and, to some extent, the uterine ligaments, and the second phenotype outside the M€ ullerian tract particularly the ovaries.”

    From Pathogenesis of deep endometriosis (2017) · cites this paper as [53]

  • The two dominant phenotypes of ectopic endometrium largely depend on the localization and have a different sex steroid hormone response.

    “The two dominant phenotypes of ectopic endometrium largely depend on the localization and have a different sex steroid hormone response (53).”

    From Pathogenesis of deep endometriosis (2017) · cites this paper as [53]

Cites

Flagged first, then by citations

1 of the 39 references couldn’t be matched to a known paper.

Cited by

Sorted by citations

Related

Authors
Brosens, I. A., & Brosens, J. J.
Affiliations
Hammersmith Hospital (GB)
ORCID
Venue
Human Reproduction
Publisher
Oxford University Press (OUP)
Published
2000-01
Volume
15
Issue
1
Pages
1-3
ISSN
  • 0268-1161 (ISSN-L)
  • 1460-2350
DOI
10.1093/humrep/15.1.1
OpenAlex
W2132050566
Cited by
69
References
39
Citations by year
2024: 1 · 2021: 1 · 2020: 1 · 2018: 2 · 2017: 3 · 2015: 1 · 2013: 2 · 2012: 2
FWCI
1.53
Type
journal article
Language
en
Open access
closed
Locations
  • Human Reproduction (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
  • Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
Keywords
endometriosis, deep infiltrating endometriosis, superficial endometriosis, disease progression, endometriosis classification, interferon-gamma, adenomyosis, endometrial bleeding, ovarian chocolate cyst
MeSH terms
Endometriosis, Female, Hormones, Humans, Ovarian Diseases, Peritoneal Diseases, Phenotype, Uterine Hemorrhage

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review