Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons
Abstract
The aim of this review was to assess critically the importance of the frequency, quantity and quality of retrograde menstruation and its relationship to peritoneal inflammation. The basis was the current evidence in women and in baboons supporting the Sampson hypothesis that retrograde menstruation is a key factor in the pathogenesis of endometriosis. It is not proven that retrograde menstruation is a universal phenomenon occurring similarly in women with and without endometriosis. A more thorough understanding of the physiological, cytological and immunological events in peritoneal fluid, peritoneum, endometrium and uterus during menstruation in women with and without endometriosis is critical in order to understand the pathogenesis of this enigmatic disease.
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Delay in diagnosis may have significant consequences in terms of disease progression.
“Unfortunately, the delay in diagnosis may have significant consequences in terms of disease progression.”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [13]
Endometriosis is more advanced in women whose diagnostic laparoscopy is delayed, supporting progression of disease over time.
“endometriosis is more advanced in women whose diagnostic laparoscopy is delayed, supporting progression of disease over time [13].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [13]
Cites
(1984) · PubMed · Cited by 997 · see citing works
Immunobiology of endometriosis
Lebovic, D. I., Mueller, M. D., & Taylor, R. N. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01630-7 · Cited by 857 · see citing works
Oosterlynck, D. J., Cornillie, F. J., Waer, M., Vandeputte, M., & Koninckx, P. R. (1991) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54414-8 · Cited by 441 · cited 1× · see citing works
“It has been hypothesized that endometriosis can be caused by decreased clearance of peritoneal ¯uid endometrial cells due to reduced natural killer (NK) activity, and/or decreased macrophage activity (Oosterlynck et al., 1991).”
BackgroundRodgers, W. H., Matrisian, L. M., Giudice, L. C., Dsupin, B. A., Cannon, P., Svitek, C., Gorstein, F., & Osteen, K. G. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117461 · Cited by 377 · see citing works
The Relation of Endometriosis to Menstrual Characteristics, Smoking, and Exercise
Cramer, D. W. (1986) · JAMA: The Journal of the American Medical Association · doi:10.1001/jama.1986.03370140102032 · Cited by 367 · see citing works
Bruner‐Tran, K. L., Matrisian, L. M., Rodgers, W. H., Gorstein, F., & Osteen, K. G. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119478 · Cited by 283 · see citing works
(1987) · PubMed · Cited by 275 · see citing works
Armenti, V. T., Ahlswede, K. M., Ahlswede, B. A., Jarrell, B. E., Moritz, M. J., & BURKE, J. F. (1994) · Transplantation · doi:10.1097/00007890-199402270-00004 · Cited by 255 · see citing works
Endometriosis: its association with retrograde menstruation, dysmenorrhoea and tubal pathology
LIU, D. T. Y., & HITCHCOCK, A. (1986) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1986.tb07995.x · Cited by 230 · see citing works
Endometrial epithelial cells in peritoneal fluid during the early follicular phase
Kruitwagen, R. F. P. M., Poels, L. G., Willemsen, W. N. P., de Ronde, I. J. Y., Jap, P. H. K., & Rolland, R. (1991) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54119-3 · Cited by 199 · see citing works
D’Hooghe, T. M., Bambra, C. S., Raeymaekers, B. M., Jonge, I. D., Lauweryns, J. M., & Koninckx, P. R. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)90180-9 · Cited by 182 · see citing works
Self-citationRetrograde menstruation in women undergoing chronic peritoneal dialysis.
Blumenkrantz, M. J., Gallagher, N., BASHORE, R. A., & Tenckhoff, H. (1981) · PubMed · Cited by 165 · see citing works
Early endometriosis invades the extracellular matrix
Spuijbroek, M. D. E. H., Dunselman, G. A. J., Menheere, P. P. C. A., & Evers, J. L. H. (1993) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(93)90482-c · Cited by 151 · see citing works
Kokorine, I., Nisolle, M., Donnez, J., Eeckhout, Y., Courtoy, P. J., & Marbaix, É. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81510-5 · Cited by 148 · see citing works
New aspects of the pathophysiology of endometriosis and associated infertility.
Koninckx, P. R., Ide, P. S., Vandenbroucke, W. V. A., & Brosens, I. A. (1980) · PubMed · Cited by 145 · see citing works
Endometrial tissue in peritoneal fluid
Bartosik, D., Jacobs, S. L., & Kelly, L. J. (1986) · Fertility and Sterility · doi:10.1016/s0015-0282(16)49813-4 · Cited by 144 · see citing works
Clinical relevance of the baboon as a model for the study of endometriosis
D’Hooghe, T. M. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00277-x · Cited by 137 · see citing works
Self-citationZhang, R., Wild, R. A., & Ojago, J. M. (1993) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55976-7 · Cited by 124 · see citing works
Menstrual characteristics in women with and without endometriosis
Vercellini, P., DEGIORGI, O., Aimi, G., Panazza, S., Uglietti, A., & Crosignani, P. (1997) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(97)00235-4 · Cited by 117 · 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-citationD’Hooghe, T. M., Bambra, C. S., Cornillie, F. J., ISAHAKIA, M. A., & Koninckx, P. R. (1991) · Biology of Reproduction · doi:10.1095/biolreprod45.3.411 · Cited by 100 · see citing works
Self-citationMenstrual characteristics associated with endometriosis
Arumugam, K., & Lim, J. M. H. (1997) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1997.tb14357.x · Cited by 94 · see citing works
Risk factors for endometriosis in the rhesus monkey (Macaca mulatta): a case-control study
Hadfield, R. (1997) · Human Reproduction Update · doi:10.1093/humupd/3.2.109 · Cited by 86 · see citing works
Symposium: reproduction in baboons. Some reproductive studies in the baboon
Stevens, V. C. (1997) · Human Reproduction Update · doi:10.1093/humupd/3.6.533 · Cited by 85 · see citing works
Endometrial cell adhesion in an in vitro model using intact amniotic membranes
van der Linden, P. J. Q., de Goeij, A. F. P. M., Dunselman, G. A. J., Erkens, H. W. H., & Evers, J. L. H. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58030-3 · Cited by 72 · see citing works
Obstructing malformations of the uterus and vagina
Pinsonneault, O., & GOLDSTEIN, D. P. (1985) · Fertility and Sterility · doi:10.1016/s0015-0282(16)48745-5 · Cited by 70 · see citing works
D’Hooghe, T. M., Bambra, C. S., Raeymaekers, B. M., & Koninckx, P. R. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58168-0 · Cited by 68 · see citing works
Self-citationWhy Do Women and Some Other Primates Menstruate?
Finn, C. A. (1987) · Perspectives in biology and medicine · doi:10.1353/pbm.1987.0007 · Cited by 61 · see citing works
D’Hooghe, T. M., Bambra, C. S., Xiao, L., Peixe, K., & Hill, J. A. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.111715 · Cited by 59 · see citing works
Self-citationD’Hooghe, T. M., Bambra, C. S., Jonge, I. D., et al. (1996) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349609033298 · Cited by 56 · see citing works
Self-citationD’Hooghe, T. M., Bambra, C. S., Raeymaekers, B. M., & Koninckx, P. R. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019537 · Cited by 52 · see citing works
Self-citationSillem, 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
D’Hooghe, T. M., Bambra, C. S., Raeymaekers, B. M., Riday, A. M., Suleman, M. A., & Koninckx, P. R. (1996) · Fertility and Sterility · doi:10.1016/s0015-0282(16)58641-5 · Cited by 48 · see citing works
Self-citationThe Mesothelium, Teflon or Velcro?
Dunselman, G. A. J., Groothuis, P. G., de Goeij, A. F. P. M., & Evers, J. L. H. (2001) · Human Reproduction · doi:10.1093/humrep/16.4.605 · Cited by 45 · see citing works
Spontaneous endometriosis in the Kenya baboon (Papio doguera)
Merrill, J. A. (1968) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(68)90572-3 · Cited by 39 · see citing works
Scheenjes, E., te Velde, E. R., & Kremer, J. (1990) · Fertility and Sterility · doi:10.1016/s0015-0282(16)53633-4 · Cited by 31 · cited 2× · see citing works
“Red-stained peritoneal ̄uid can be observed not only during menstruation, but also during the ®rst 5 days after ovulation (Scheenjes et al., 1990) and during other phases of the”
BackgroundWild, R. A., Zhang, R., & Medders, D. (1994) · Journal of the Society for Gynecologic Investigation · doi:10.1177/107155769400100113 · Cited by 29 · see citing works
Endometriosis in a baboon (Papio doguera).
Folse, D. S., & Stout, L. C. (1978) · PubMed · Cited by 29 · see citing works
Cycle Fecundity in Baboons of Proven Fertility with Minimal Endometriosis
́Hooghe, T. D., Bambra, C. S., & Koninckx, P. R. (2010) · Gynecologic and Obstetric Investigation · doi:10.1159/000292524 · Cited by 27 · see citing works
The Acute Clinical Features of Retrograde Menstruation
Reti, L. L., Byrne, G. D., & Davoren, R. A. M. (1983) · Australian and New Zealand Journal of Obstetrics and Gynaecology · doi:10.1111/j.1479-828x.1983.tb00160.x · Cited by 24 · see citing works
Immunobiology of endometriosis
D’Hooghe, T. M., & Hill, J. E. (1996) · Cited by 20 · see citing works
Self-citationLack of effect of peritoneal endometriosis on fertility in the rabbit model
Dunselman, G. A. J., Dumoulin, J. C. M., Land, J. A., et al. (1991) · Fertility and Sterility · doi:10.1016/s0015-0282(16)54496-3 · Cited by 15 · see citing works
Endometriosis with bacterial peritonitis in a baboon.
DaRif, C. A., Rf, P., & Tr, S. (1984) · PubMed · Cited by 9 · see citing works
D’Hooghe, T. M., Bambra, C. S., & Hill, J. A. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81883-3 · Cited by 4 · see citing works
Self-citationQuantity and Quality of Retrograde Menstruation: Red Blood Cells, Inflammation and Peritoneal Cells
Debrock, S., Drijkoningen, M., Goossens, W., et al. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01054-2 · Cited by 3 · see citing works
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Sorted by citations
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772 · see citing works
Bulun, S. E., Yilmaz, B. D., Sison, C., Miyazaki, K., Bernardi, L., Liu, S., Kohlmeier, A., Yin, P., Milad, M., & Wei, J. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00242 · Cited by 844 · see citing works
The Main Theories on the Pathogenesis of Endometriosis
Lamceva, J., Uljanovs, R., & Strumfa, I. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054254 · Cited by 324 · see citing works
Potential involvement of the immune system in the development of endometriosis
Kyama, C. M., Debrock, S., Mwenda, J. M., & D'Hooghe, T. M. (2003) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-1-123 · Cited by 244 · see citing works
Self-citationPotential involvement of iron in the pathogenesis of peritoneal endometriosis
Defrere, S., Lousse, J. C., Gonzalez-Ramos, R., Colette, S., Donnez, J., & Van Langendonckt, A. (2008) · Molecular Human Reproduction · doi:10.1093/molehr/gan033 · Cited by 204 · see citing works
Update on biomarkers for the detection of endometriosis
Fassbender, A., Burney, R. O., F. O, D., D’Hooghe, T., & Giudice, L. (2015) · BioMed Research International · doi:10.1155/2015/130854 · Cited by 195 · see citing works
“Endometriosis is histologically characterized by the displacement of endometrial tissue to extrauterine locations including the pelvic peritoneum, ovaries, and bowel.”
BackgroundSelf-citationEvaluation of a panel of 28 biomarkers for the non-invasive diagnosis of endometriosis
Vodolazkaia, A., El-Aalamat, Y., Popovic, D., Mihalyi, A., Bossuyt, X., Kyama, C. M., Fassbender, A., Bokor, A., Schols, D., Huskens, D., et al. (2012) · Human Reproduction · doi:10.1093/humrep/des234 · Cited by 189 · see citing works
Self-citationDiagnosis and management of endometriosis: summary of NICE guidance
Kuznetsov, L., Dworzynski, K., Davies, M., & Overton, C. (2017) · BMJ · doi:10.1136/bmj.j3935 · Cited by 181 · see citing works
Molecular classification of endometriosis and disease stage using high-dimensional genomic data
Tamaresis, J. S., Irwin, J. C., Goldfien, G. A., Rabban, J. T., Burney, R. O., Nezhat, C., DePaolo, L. V., & Giudice, L. C. (2014) · Endocrinology · doi:10.1210/en.2014-1490 · Cited by 168 · see citing works
Non-invasive diagnosis of endometriosis based on a combined analysis of six plasma biomarkers
Mihalyi, A., Gevaert, O., Kyama, C. M., Simsa, P., Pochet, N., De Smet, F., De Moor, B., Meuleman, C., Billen, J., Blanckaert, N., et al. (2010) · Human Reproduction · doi:10.1093/humrep/dep425 · Cited by 161 · see citing works
Self-citationMenstruation pulls the trigger for inflammation and pain in endometriosis
Laux-Biehlmann, A., d’Hooghe, T., & Zollner, T. M. (2015) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2015.03.004 · Cited by 150 · see citing works
Self-citationFassbender, A., Vodolazkaia, A., Saunders, P., Lebovic, D., Waelkens, E., De Moor, B., & D'Hooghe, T. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.01.097 · Cited by 150 · see citing works
Self-citationThe Role of the Lymphatic System in Endometriosis: A Comprehensive Review of the Literature1
Jerman, L. F., & Hey-Cunningham, A. J. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.114.124313 · Cited by 122 · see citing works
Fassbender, A., Verbeeck, N., Börnigen, D., Kyama, C. M., Bokor, A., Vodolazkaia, A., Peeraer, K., Tomassetti, C., Meuleman, C., Gevaert, O., et al. (2012) · Human Reproduction · doi:10.1093/humrep/des127 · Cited by 87 · see citing works
Self-citationLin, W.-C., Chang, C. Y.-Y., Hsu, Y.-A., Chiang, J.-H., & Wan, L. (2016) · Medicine · doi:10.1097/md.0000000000002773 · Cited by 70 · see citing works
The known, the unknown and the future of the pathophysiology of endometriosis
Ochoa Bernal, M. A., & Fazleabas, A. T. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115815 · Cited by 59 · see citing works
“One possible hypothesis is that endometriosis can be caused by the decreased clearance of the endometrial cells and fragments due to reduced natural killer (NK) activity, and/or decreased macrophage activity [20,21].”
BackgroundInfluentialProteomics Analysis of Plasma for Early Diagnosis of Endometriosis
Fassbender, A., Waelkens, E., Verbeeck, N., Kyama, C. M., Bokor, A., Vodolazkaia, A., Van de Plas, R., Meuleman, C., Peeraer, K., Tomassetti, C., et al. (2012) · Obstetrics & Gynecology · doi:10.1097/aog.0b013e31823fda8d · Cited by 51 · see citing works
Self-citationSharpe-Timms, K. L., Nabli, H., Zimmer, R. L., Birt, J. A., & Davis, J. W. (2010) · Human Reproduction · doi:10.1093/humrep/deq032 · Cited by 43 · see citing works
Pathological functions of hypoxia in endometriosis
Hsiao, K.-Y. (2015) · Frontiers in Bioscience · doi:10.2741/e736 · Cited by 61 · see citing works
Overall Adiposity, Adipose Tissue Distribution, and Endometriosis: A Systematic Review
Backonja, U., Buck Louis, G. M., & Lauver, D. R. (2016) · Nursing Research · doi:10.1097/nnr.0000000000000146 · Cited by 39 · see citing works
Biomarker development in endometriosis
Burney, R. O. (2014) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.3109/00365513.2014.936692 · Cited by 16 · see citing works
Sapmaz, T., Coskun, G., Saker, D., Pence, H. H., Keles, P., Hayretdag, C., Kuras, S., Topkaraoglu, S., Erdem, E., Efendic, F., et al. (2022) · Pathology - Research and Practice · doi:10.1016/j.prp.2022.153951 · Cited by 15 · see citing works
Lousse, J.-C., Defrère, S., Ramos, R. G., Van Langendonckt, A., Colette, S., & Donnez, J. (2009) · Journal of Endometriosis · doi:10.1177/228402650900100104 · Cited by 10 · see citing works
Kasai, K., Kato, T., Kadota, Y., Erdenebayar, O., Keyama, K., Kawakita, T., Yoshida, K., Kuwahara, A., Matsuzaki, T., & Irahara, M. (2019) · The Journal of Medical Investigation · doi:10.2152/jmi.66.123 · Cited by 9 · see citing works
- Authors
- D'Hooghe, T. M.
- Venue
- Human Reproduction Update
- Publisher
- Oxford University Press (OUP)
- Published
- 2002-01-01
- Volume
- 8
- Issue
- 1
- Pages
- 84-88
- ISSN
- 1355-4786 (ISSN-L)
- 1460-2369
- OpenAlex
- W2143537649
- Cited by
- 231
- References
- 45
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 17 · 2023: 13 · 2022: 8 · 2021: 8 · 2020: 12 · 2019: 14 · 2018: 1 · 2017: 9 · 2016: 15 · 2015: 9 · 2014: 15 · 2013: 19 · 2012: 13
- FWCI
- 5.71
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction Update (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Menstrual Health and Disorders
- Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
- Keywords
- endometriosis, retrograde menstruation, peritonitis, endometriosis pathogenesis, baboons, peritoneal fluid, menstrual physiology
- MeSH terms
- Animals, Disease Models, Animal, Endometriosis, Female, Humans, Menstruation Disturbances, Papio, Peritonitis, Prevalence
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