Smooth muscles are frequent components of endometriotic lesions
Abstract
Deep infiltrating endometriosis (deeper than 5 mm under the peritoneum) often takes the form of a nodular lesion (or 'adenomyotic nodule') consisting of smooth muscles and fibrosis with active glands and scanty stroma. Thus, among endometriotic lesions, a certain distinction is drawn between musculo-glandular lesions and glandular lesions composed of endometrial-like epithelium surrounded by a cell-producing (cytogenous) stroma. The aim of this study was to detect by immunohistochemistry, with a monoclonal antibody against muscle-specific actin, the presence of smooth muscles in 54 endometriotic lesions originating from four different pelvic locations (peritoneum, ovary, rectovaginal septum and uterosacral ligaments) and to quantify the smooth muscle content. Smooth muscles were frequent components of endometriotic lesions in pelvic locations. In addition, smooth muscles were significantly (P < 0. 001) more abundant in endometriotic lesions than in their respective unaffected sites. This finding supports, at least partially, the occurrence of a metaplastic phenomenon in the pathogenesis of endometriotic lesions. The definition of distinct endometriotic entities based on the difference in the tissue composition of the lesions (endometriotic nodules versus adenomyotic nodules) is inconsistent with the very frequent presence of smooth muscle cells in endometriosis irrespective of its localization.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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 genetic/epigenetic theory makes it conceivable that the fibrosis surrounding deep endometriosis lesions and eventually the outer cell layers might be composed of normal cells with reversible metaplastic changes induced by the endometriosis lesion through cell-cell interaction.
“The genetic/epigenetic theory makes it conceivable that the fibrosis surrounding deep endometriosis lesions and eventually the outer cell layers might be composed of normal cells with reversible ''metaplastic'' changes induced by the endometriosis lesion through cell-cell interaction (260).”
From Pathogenesis of endometriosis: The genetic/epigenetic theory (2019) · cites this paper as [260]
DE lesions typically have higher fibromuscular content than ovarian endometriomas (OE) lesions.
“DE lesions typically have higher fibromuscular content than that of ovarian endometriomas (OE) lesions, but the underlying reason remains elusive.”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [15]
DE is characterized by the presence of smooth muscle metaplasia (SMM) and a high degree of fibrotic tissues.
“One feature that DE stands out from other subtypes of endometriosis is its presence of smooth muscle metaplasia (SMM) and its high degree of fibrotic tissues4,15–17”
From Neuropeptides Substance P and Calcitonin Gene Related Peptide Accelerate the Development and Fibrogenesis of Endometriosis (2019) · cites this paper as [15]
The definition of distinct endometriotic entities based on the difference in the tissue composition of the lesions (endometriotic nodules vs. adenomyotic nodules) is inconsistent with the very frequent presence of smooth muscle cells in endometriosis irrespective of its localization.
“Anaf et al. (45) concluded that the definition of distinct endometriotic entities based on the difference in the tissue composition of the lesions (endometriotic nodules vs. adenomyotic nodules) is inconsistent with the very frequent presence of smooth muscle cells in endometriosis irrespective of its localization.”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [45]
The metaplastic phenomenon in the pathogenesis of deep infiltrating endometriosis, whether located in peritoneum, ovary, rectovaginal septum, or uterosacral ligament, was at least partially confirmed by immunohistochemical studies.
“The metaplastic phenomenon in the pathogenesis of deep infiltrating endometriosis, whether located in peritoneum, ovary, rectovaginal septum, or uterosacral ligament was at least partially confirmed by immunohistochemical studies (45).”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [45]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Firminger, H. I. (1968) · Armed Forces Institute of Pathology eBooks · Cited by 3,041 · see citing works
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334 · see citing works
Nisolle, M., & Donnez, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00191-x · Cited by 1,279 · see citing works
Deeply infiltrating pelvic endometriosis: histology and clinical significance
Cornillie, F. J., Oosterlynck, D., Lauweryns, J. M., & Koninckx, P. R. (1990) · Fertility and Sterility · doi:10.1016/s0015-0282(16)53570-5 · Cited by 594 · see citing works
Aromatase expression in endometriosis.
Noble, L. S., Simpson, E. R., Johns, A., & Bulun, S. E. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.1.8550748 · Cited by 566 · see citing works
Vascular endothelial growth factor (VEGF) in endometriosis
Donnez, J., Smoes, P., Gillerot, S., Casanas-Roux, F., & Nisolle, M. (1998) · Human Reproduction · doi:10.1093/humrep/13.6.1686 · Cited by 531 · see citing works
Aberrant integrin expression in the endometrium of women with endometriosis
Lessey, B. A., Castelbaum, A. J., Sawin, S. W., Buck, C. A., Schinnar, R., Bilker, W. B., & Strom, B. L. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.2.7519194 · Cited by 514 · see citing works
The secondary Müllerian system.
Lauchlan, S. (1972) · Obstetrical and Gynecological Survey · doi:10.1097/00006254-197203000-00001 · Cited by 371 · see citing works
Kitawaki, J., Noguchi, T., Amatsu, T., Maeda, K., Tsukamoto, K., Yamamoto, T., Fushiki, S., Osawa, Y., & Honjo, H. (1997) · Biology of Reproduction · doi:10.1095/biolreprod57.3.514 · Cited by 305 · see citing works
Prostaglandin E2 Stimulates Aromatase Expression in Endometriosis-Derived Stromal Cells
Noble, L. S. (1997) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.82.2.600 · Cited by 301 · 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
Tumors of the uterine corpus and gestational trophoblastic disease
Silverberg, S. G., Kurman, R. J., Norris, H. J., et al. (1992) · Armed Forces Institute of Pathology eBooks · Cited by 179 · see citing works
Donnez, J., Nisolle, M., Casanas-Roux, F., Bassil, S., & Anaf, V. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136001 · Cited by 175 · cited 2× · see citing works
“Some authors found the presence of abundant smooth muscle cells in this area (Donnez et al., 1995).”
BackgroundSelf-citationAngiongenesis: a new theory for endometriosis
Healy, D. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.736 · Cited by 173 · see citing works
Cell proliferation is increased in the endometrium of women with endometriosis
Wingfield, M. B., Macpherson, A., Healy, D. L., & Rogers, P. A. W. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57733-4 · Cited by 155 · see citing works
Flieder, D. B., Moran, C. A., Travis, W. D., Koss, M. N., & Mark, E. J. (1998) · Human Pathology · doi:10.1016/s0046-8177(98)90021-1 · Cited by 143 · see citing works
THE HISTOGENESIS OF ENDOMETRIOSIS
Ridley, J. H. (1968) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-196801000-00001 · Cited by 135 · see citing works
THE PATHOGENESIS OF ENDOMETRIOSIS
Levander, G., & NORMANN, P. (1955) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016345509158287 · Cited by 119 · see citing works
Theories on the pathogenesis of endometriosis
van der Linden, P. J. Q. (1996) · Human Reproduction · doi:10.1093/humrep/11.suppl_3.53 · Cited by 115 · see citing works
Evidence for estrogen synthesis in adenomyotic tissues
Yamamoto, T., Noguchi, T., Tamura, T., Kitawaki, J., & Okada, H. (1993) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(93)90654-2 · Cited by 111 · see citing works
Leiomyomatosis Peritonealis Disseminata
Fujii, S., Okamura, H., NAKASHIMA, N., et al. (1980) · Obstetrics and Gynecology · doi:10.1097/00006250-198003001-00025 · Cited by 86 · see citing works
Progesterone-induced smooth muscle—like cells in the subperitoneal nodules produced by estrogen
Fujii, S., Nakashima, N., Okamura, H., Takenaka, A., Kanzaki, H., Okuda, Y., Morimoto, K., & Nishimura, T. (1981) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(81)90440-3 · Cited by 57 · see citing works
Fibrogenesis in Peritoneal Endometriosis
Matsuzaki, S., Canis, M. J., Darcha, C., Dechelotte, P., Pouly, J. L., & Bruhat, M. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000010094 · Cited by 52 · see citing works
Sillem, M., Hahn, U., Coddington, C. C., et al. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58521-5 · Cited by 52 · see citing works
The histogenesis of endometriosis
Jh, R. (1968) · Obstetrical & Gynecological Survey · Cited by 45 · see citing works
The association of intrauterine filling defects on hysterosalpingogram with endometriosis
McBean, J. H., Gibson, M., & Brumsted, J. R. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58562-8 · Cited by 40 · cited 2× · see citing works
“These range from gross morphological changes such as the polypoid appearance of the endometrium at hysterosalpingography (McBean et al., 1996), to changes in immunocytochemistry such as aberrant integrin expression (Lessey et al., 1994), and biochemical changes such as overexpression of plasminogen…”
BackgroundPathology of the fallopian tube, broad ligament, peritoneum, and pelvic soft tissues
Thor, A. D., Young, R. H., & Clement, P. B. (1991) · Human Pathology · doi:10.1016/0046-8177(91)90174-n · Cited by 38 · see citing works
New principles in the management of endometriosis.
Brosens, I. A. (1994) · PubMed · Cited by 35 · see citing works
Préfontaine, M., Shih, C., Pan, C. C., et al. (1990) · Journal of Endocrinology · doi:10.1677/joe.0.1270539 · Cited by 27 · see citing works
Embryology of the Female Genital Tract
Parmley, T. H. (1987) · Springer eBooks · doi:10.1007/978-1-4757-1942-0_1 · Cited by 24 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Rosai, J. (ed.) (1996) Ackerman's Surgical Pathology , 8th edn. Mosby, St Louis, pp. 2146-2148.
Cited by
Sorted by citations
Endometriosis: epidemiology and aetiological factors
Viganò, P., Parazzini, F., Somigliana, E., & Vercellini, P. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.01.007 · Cited by 718 · see citing works
Deep Pelvic Endometriosis: MR Imaging for Diagnosis and Prediction of Extension of Disease
Bazot, M., Darai, E., Hourani, R., Thomassin, I., Cortez, A., Uzan, S., & Buy, J.-N. (2004) · Radiology · doi:10.1148/radiol.2322030762 · Cited by 580 · see citing works
Pathogenesis of endometriosis: The genetic/epigenetic theory
Koninckx, P. R., Ussia, A., Adamyan, L., Wattiez, A., Gomel, V., & Martin, D. C. (2019) · Fertility and Sterility · doi:10.1016/j.fertnstert.2018.10.013 · Cited by 427 · see citing works
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
Self-citationEndometriosis results from the dislocation of basal endometrium
Leyendecker, G. (2002) · Human Reproduction · doi:10.1093/humrep/17.10.2725 · Cited by 300 · 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
Time to redefine endometriosis including its pro-fibrotic nature
Vigano, P., Candiani, M., Monno, A., Giacomini, E., Vercellini, P., & Somigliana, E. (2018) · Human Reproduction · doi:10.1093/humrep/dex354 · Cited by 235 · 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
Findings of Pelvic Endometriosis at Transvaginal US, MR Imaging, and Laparoscopy
Chamié, L. P., Blasbalg, R., Pereira, R. M. A., Warmbrand, G., & Serafini, P. C. (2011) · RadioGraphics · doi:10.1148/rg.314105193 · Cited by 219 · see citing works
Dyson, M. T., Roqueiro, D., Monsivais, D., Ercan, C. M., Pavone, M. E., Brooks, D. C., Kakinuma, T., Ono, M., Jafari, N., Dai, Y., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004158 · Cited by 211 · see citing works
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
Leone Roberti Maggiore, U., Ferrero, S., Candiani, M., Somigliana, E., Viganò, P., & Vercellini, P. (2017) · European Urology · doi:10.1016/j.eururo.2016.12.015 · Cited by 187 · see citing works
A new concept of endometriosis and adenomyosis, tissue injury and repair (TIAR)
Leyendecker, G., & Wildt, L. (2011) · hmbci · doi:10.1515/hmbci.2011.002 · Cited by 147 · see citing works
Somigliana, E. (2004) · Human Reproduction · doi:10.1093/humrep/deg513 · Cited by 115 · see citing works
Liu, X., Zhang, Q., & Guo, S.-W. (2018) · Reproductive Sciences · doi:10.1177/1933719117718275 · Cited by 110 · see citing works
Fibrosis and smooth muscle metaplasia in rectovaginal endometriosis
Itoga, T., Matsumoto, T., Takeuchi, H., Yamasaki, S., Sasahara, N., Hoshi, T., & Kinoshita, K. (2003) · Pathology International · doi:10.1046/j.1440-1827.2003.01483.x · Cited by 108 · see citing works
Stem cell theory for the pathogenesis of endometriosis
Maruyama, T. (2012) · Frontiers in Bioscience · doi:10.2741/e589 · Cited by 109 · see citing works
Is rectovaginal endometriosis a progressive disease?
Fedele, L., Bianchi, S., Zanconato, G., Raffaelli, R., & Berlanda, N. (2004) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.06.104 · Cited by 101 · see citing works
Yan, D., Liu, X., & Guo, S.-W. (2019) · Scientific Reports · doi:10.1038/s41598-019-39170-w · Cited by 82 · see citing works
Mechsner, S., Bartley, J., Loddenkemper, C., Salomon, D. S., Starzinski-Powitz, A., & Ebert, A. D. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.11.038 · Cited by 79 · see citing works
van Kaam, K. J. A. F., Schouten, J. P., Nap, A. W., Dunselman, G. A. J., & Groothuis, P. G. (2008) · Human Reproduction · doi:10.1093/humrep/den153 · Cited by 70 · see citing works
Role of medical therapy in the management of deep rectovaginal endometriosis
Vercellini, P., Buggio, L., & Somigliana, E. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.08.038 · Cited by 62 · see citing works
Ibrahim, M. G., Sillem, M., Plendl, J., Chiantera, V., Sehouli, J., & Mechsner, S. (2017) · Reproductive Sciences · doi:10.1177/1933719116687855 · Cited by 52 · see citing works
Kyama, C. M., T’Jampens, D., Mihalyi, A., Simsa, P., Debrock, S., Waelkens, E., Landuyt, B., Meuleman, C., Fulop, V., Mwenda, J. M., et al. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.12.024 · Cited by 46 · see citing works
Estrogen and progesterone receptors in smooth muscle component of deep infiltrating endometriosis
Noël, J.-C., Chapron, C., Bucella, D., Buxant, F., Peny, M.-O., Fayt, I., Borghese, B., & Anaf, V. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.12.114 · Cited by 41 · see citing works
Self-citationVercellini, P., Buggio, L., Borghi, A., Monti, E., Gattei, U., & Frattaruolo, M. P. (2018) · Acta Obstetricia et Gynecologica Scandinavica · doi:10.1111/aogs.13328 · Cited by 39 · see citing works
Could statins constitute a novel treatment for endometriosis? Systematic review of the literature
Gibran, L., Maranhão, R. C., Abrão, M. S., Baracat, E. C., & Podgaec, S. (2014) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.05.028 · Cited by 29 · see citing works
New treatment strategies and emerging drugs in endometriosis
Streuli, I., de Ziegler, D., Borghese, B., Santulli, P., Batteux, F., & Chapron, C. (2012) · Expert Opinion on Emerging Drugs · doi:10.1517/14728214.2012.668885 · Cited by 27 · see citing works
Nezhat, C. R., Oskotsky, T. T., Robinson, J. F., Fisher, S. J., Tsuei, A., Liu, B., Irwin, J. C., Gaudilliere, B., Sirota, M., Stevenson, D. K., et al. (2025) · npj Women s Health · doi:10.1038/s44294-024-00052-w · Cited by 25 · see citing works
Rectus Abdominis Muscle Endometriosis: A Unique Case Report with a Literature Review
Turčić, M., Matušan Ilijaš, K., Rajković Molek, K., & Valković Zujić, P. (2025) · Current Issues in Molecular Biology · doi:10.3390/cimb47010047 · Cited by 6 · see citing works
- Authors
- Anaf, V.
- Affiliations
- Université Libre de Bruxelles (BE)
- Corresponding author
- Anaf, V.
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2000-04-01
- Volume
- 15
- Issue
- 4
- Pages
- 767-771
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2117538656
- Cited by
- 183
- References
- 30
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 3 · 2023: 10 · 2022: 5 · 2021: 8 · 2020: 8 · 2019: 6 · 2018: 8 · 2017: 9 · 2016: 4 · 2015: 11 · 2014: 10 · 2013: 6 · 2012: 9
- FWCI
- 5.47
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (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
- deep infiltrating endometriosis, smooth muscle, muscle-specific actin, metaplasia, endometriosis pathogenesis, ovary, rectovaginal septum, uterosacral ligament, peritoneum
- MeSH terms
- Actins, Adult, Antibodies, Monoclonal, Endometriosis, Female, Humans, Immunohistochemistry, Ligaments, Muscle, Smooth, Ovary, Peritoneum, Rectum, Sacrum, Staining and Labeling, Uterus, Vagina
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
