Tissue integrity is essential for ectopic implantation of human endometrium in the chicken chorioallantoic membrane
Abstract
BACKGROUND: Not all women with patent tubes develop clinically manifest endometriosis. Quality and quantity of endometrium in retrograde menstruation may be the determining factor in the development of the disease. We hypothesize that retrograde shedding of endometrial fragments with preserved integrity facilitates implantation of endometrium in ectopic locations, resulting in endometriotic lesion development. We evaluate the impact of tissue integrity on the success of endometriosis-like lesion development in the chicken embryo chorioallantoic membrane (CAM) model. METHODS: Menstrual and non-menstrual (cyclic) endometrium were collected by biopsy, and either minced or enzymatically dispersed. Spontaneously shed menstrual effluent was collected by a menstrual cup, and cells and tissue were isolated. We evaluated whether infiltration or lesion formation in the CAM occurred after transplantation of endometrium onto the CAM. RESULTS: Transplantation of biopsied menstrual and cyclic endometrium fragments, and of endometrium fragments >1 mm(3) isolated from menstrual effluent, resulted in lesion formation. Transplantation of endometrial cells isolated from menstrual effluent did not lead to lesion formation. After transplantation of digested biopsied cyclic endometrium, infiltration in the CAM but no lesions were observed. CONCLUSION: In the CAM assay, integrity of tissue architecture determines success of implantation of human endometrium in ectopic locations.
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For development on the chicken allantoic membrane, tissue integrity is important.
“For development on the chicken allantoic membrane, tissue integrity is important (115).”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [115]
These experiments emphasize the importance of tissue integrity and of the special relationship of endometrium and junctional zone for growth and development.
“These experiments, however, emphasize the importance of tissue integrity-as for the chicken allantoic membrane experiments (115)-and of the special relationship of endometrium and junctional zone for growth and development.”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [115]
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Cites
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
Endometriosis in association with uterine anomaly
Sanfilippo, J. S., Wakim, N. G., Schikler, K. N., & Yussman, M. A. (1986) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(86)90389-3 · Cited by 270 · see citing works
Menstrual Cycle Characteristics and the Risk of Endometriosis
Darrow, S. L., Vena, J., Batt, R., Zielezny, M., Michalek, A., & Selman, S. (1993) · Epidemiology · doi:10.1097/00001648-199303000-00009 · Cited by 169 · see citing works
Jones, R. K., Bulmer, J. N., & Searle, R. F. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a135901 · Cited by 129 · see citing works
Marbaix, É., Kokorine, I., Henriet, P., Donnez, J., Courtoy, P. J., & Eeckhout, Y. (1995) · Biochemical Journal · doi:10.1042/bj3051027 · Cited by 111 · see citing works
Development of a model of retrograde menstruation in baboons (Papio anubis)
D’Hooghe, T. M., Bambra, C. S., Suleman, M. A., Dunselman, G. A. J., Evers, H., & Koninckx, P. R. (1994) · Fertility and Sterility · doi:10.1016/s0015-0282(16)56957-x · Cited by 108 · see citing works
Self-citationArmstrong, P. B., Quigley, J. P., & Sidebottom, E. (1982) · PubMed · Cited by 106 · see citing works
TRANSPLANTABILITY OF MALIGNANT TUMORS TO THE EMBRYOS OF A FOREIGN SPECIES
MURPHY, J. B. (1912) · JAMA · doi:10.1001/jama.1912.04270090118016 · Cited by 100 · see citing works
Scher, C. D., Haudenschild, C. C., & Klagsbrun, M. (1976) · Cell · doi:10.1016/0092-8674(76)90149-5 · Cited by 80 · see citing works
Reduced proliferation and cell adhesion in endometriosis
Scotti, S. (2000) · Molecular Human Reproduction · doi:10.1093/molehr/6.7.610 · Cited by 75 · see citing works
Koks, C. A. M. (1999) · Human Reproduction · doi:10.1093/humrep/14.3.816 · Cited by 71 · 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
Evaluation of a menstrual cup to collect shed endometrium for in vitro studies
Koks, C. A. M., Dunselman, G. A. J., de Goeij, A. F. P. M., et al. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00250-1 · Cited by 49 · see citing works
Self-citationKoks, C. A. M., Groothuis, P. G., Slaats, P., et al. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00566-x · Cited by 49 · see citing works
Self-citationMaas, J. W. M., Groothuis, P. G., Dunselman, G. A. J., de Goeij, A. F. P. M., Struijker-Boudier, H. A. J., & Evers, J. L. H. (2001) · Human Reproduction · doi:10.1093/humrep/16.4.627 · Cited by 49 · see citing works
Self-citationThe defense against endometriosis
Evers, J. L. H. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58499-4 · Cited by 16 · see citing works
Self-citationWhat is the most appropriate phase of endometrium to use for peritoneal attachment studies?
Groothuis, P. (1999) · PubMed · Cited by 2 · see citing works
Self-citation(1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00245-9 · Cited by 1 · see citing works
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Pathogenesis and pathophysiology of endometriosis
Burney, R. O., & Giudice, L. C. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.06.029 · Cited by 1,590 · 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
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
Nap, A. W., Groothuis, P. G., Demir, A. Y., Evers, J. L. H., & Dunselman, G. A. J. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.01.005 · Cited by 138 · see citing works
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- Authors
- Nap, A. W., Groothuis, P. G., Demir, A. Y., Maas, J. W. M., Dunselman, G. A. J., de Goeij, A. F. P. M., & Evers, J. L. H.
- Affiliations
- Maastricht University Medical Centre (NL)
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2003-01-01
- Volume
- 18
- Issue
- 1
- Pages
- 30-34
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2169469417
- Cited by
- 55
- References
- 18
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 2 · 2023: 3 · 2022: 3 · 2021: 1 · 2020: 3 · 2019: 3 · 2018: 2 · 2017: 1 · 2016: 2 · 2015: 2 · 2014: 1 · 2013: 2 · 2012: 2
- FWCI
- 2.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (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 › Public Health, Environmental and Occupational Health › Menstrual Health and Disorders
- Keywords
- endometriosis, tissue integrity, chorioallantoic membrane model, retrograde menstruation, endometrium
- MeSH terms
- Allantois, Animals, Cell Division, Chick Embryo, Chorion, Endometriosis, Endometrium, Female, Humans, Menstruation, Transplantation, Heterologous, Transplantation, Heterotopic
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