Potential involvement of iron in the pathogenesis of peritoneal endometriosis
Abstract
The aim of this study is to review the current literature associating endometriosis with iron and to discuss the potential causes and consequences of iron overload in the pelvic cavity. Indeed, iron is essential for all living organisms. However, excess iron can result in toxicity and is associated with pathological disorders. In endometriosis patients, iron overload has been demonstrated in the different components of the peritoneal cavity (peritoneal fluid, endometriotic lesions, peritoneum and macrophages). Animal models allow us to gather essential information on the origin, metabolism and effect of iron overload in endometriosis, which may originate from erythrocytes carried into the pelvic cavity mainly by retrograde menstruation. Peritoneal macrophages play an important role in the degradation of these erythrocytes and in subsequent peritoneal iron metabolism. Iron overload could affect a wide range of mechanisms involved in endometriosis development, such as oxidative stress or lesion proliferation. In conclusion, excess iron accumulation can result in toxicity and may be one of the factors contributing to the development of endometriosis. Treatment with an iron chelator could thus be beneficial in endometriosis patients to prevent iron overload in the pelvic cavity, thereby diminishing its deleterious effect.
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Endometriosis also occurs in patients after menopause and in adolescent women.
“However, it should be noted that there are also cases of patients with endometriosis after menopause, and it also happens in adolescent women [17].”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [17]
Endometriosis affects 10-15% of women of reproductive age and 35-50% of women with pelvic pain and/or infertility.
“This disease affects from 10–15% of women of reproductive age and 35–50% of women with pelvic pain and/or infertility.”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [17]
Cites
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · see citing works
THE HEME OXYGENASE SYSTEM:A Regulator of Second Messenger Gases
Maines, M. D. (1997) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.37.1.517 · Cited by 2,489 · 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
Andrews, N. C. (1999) · New England Journal of Medicine · doi:10.1056/nejm199912233412607 · Cited by 2,130 · see citing works
Identification of the haemoglobin scavenger receptor
Kristiansen, M., Graversen, J. H., Jacobsen, C., Sonne, O., Hoffman, H.-J., Law, S. K. A., & Moestrup, S. K. (2001) · Nature · doi:10.1038/35051594 · Cited by 1,712 · see citing works
Phosphorylation of NF-κB and IκB proteins: implications in cancer and inflammation
Viatour, P., Merville, M., Bours, V., & Chariot, A. (2004) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2004.11.009 · Cited by 1,497 · see citing works
McKie, A. T., Marciani, P., Rolfs, A., Brennan, K., Wehr, K., Barrow, D., Miret, S., Bomford, A., Peters, T. J., Farzaneh, F., et al. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80425-6 · Cited by 1,422 · see citing works
Toxicity of iron and hydrogen peroxide: the Fenton reaction
Winterbourn, C. C. (1995) · Toxicology Letters · doi:10.1016/0378-4274(95)03532-x · Cited by 1,415 · see citing works
Mechanisms of brain injury after intracerebral haemorrhage
Xi, G., Keep, R. F., & Hoff, J. T. (2005) · The Lancet Neurology · doi:10.1016/s1474-4422(05)70283-0 · Cited by 1,365 · 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
REGULATION OF GENE EXPRESSION BY REACTIVE OXYGEN
Dalton, T. P., Shertzer, H. G., & Puga, A. (1999) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.39.1.67 · Cited by 1,112 · see citing works
An iron-regulated ferric reductase associated with the absorption of dietary iron
McKie, A. T., Barrow, D., Latunde-Dada, G. O., Rolfs, A., Sager, G., Mudaly, E., Mudaly, M., Richardson, C., Barlow, D., Bomford, A., et al. (2001) · Science · doi:10.1126/science.1057206 · Cited by 1,101 · see citing works
Ferritin: a cytoprotective antioxidant strategem of endothelium.
Balla, G., Jacob, H., Balla, J., Rosenberg, M. E., Nath, K. A., Apple, F., Eaton, J. W., & Vercellotti, G. M. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)37165-0 · Cited by 1,097 · see citing works
Vulpe, C. D., Kuo, Y.-M., Murphy, T. L., Cowley, L., Askwith, C., Libina, N., Gitschier, J., & Anderson, G. J. (1999) · Nature Genetics · doi:10.1038/5979 · Cited by 1,084 · see citing works
(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
Antioxidant activity of albumin-bound bilirubin.
Stocker, R., Glazer, A. N., & Ames, B. N. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.16.5918 · Cited by 769 · see citing works
Bothwell, T. H., Charlton, R. W., Cook, J. D., & Finch, C. A. (1979) · Blackwell Scientific Publications eBooks · Cited by 730 · see citing works
Different Faces of the Heme-Heme Oxygenase System in Inflammation
Wagener, F. A. D. T. G., Volk, H., Willis, D., Abraham, N. G., Soares, M. P., Adema, G. J., & Figdor, C. G. (2003) · Pharmacological Reviews · doi:10.1124/pr.55.3.5 · Cited by 537 · 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
Self-citationMolecular and cellular mechanisms of iron homeostasis and toxicity in mammalian cells
Crichton, R. R., Wilmet, S., Legssyer, R., & Ward, R. J. (2002) · Journal of Inorganic Biochemistry · doi:10.1016/s0162-0134(02)00461-0 · Cited by 494 · see citing works
The role of iron in cell cycle progression and the proliferation of neoplastic cells
Le, N. (2002) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/s0304-419x(02)00068-9 · Cited by 453 · see citing works
Aisen, P., Wessling‐Resnick, M., & Leibold, E. A. (1999) · Current Opinion in Chemical Biology · doi:10.1016/s1367-5931(99)80033-7 · Cited by 424 · see citing works
Biochimica et biophysica acta. Protein structure and molecular enzymology
ScienceDirect (2002) · Cited by 395 · see citing works
Peritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis
Gazvani, R., & Templeton, A. (2002) · Reproduction · doi:10.1530/rep.0.1230217 · Cited by 393 · see citing works
Oxidative stress and peritoneal endometriosis
Van Langendonckt, A., Casanas-Roux, F., & Donnez, J. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)02959-x · Cited by 391 · see citing works
Self-citationThe 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
Iron Metabolism in the Reticuloendothelial System
Knutson, M. D., & Wessling‐Resnick, M. (2003) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/713609210 · Cited by 349 · see citing works
Yamaguchi, K., Mandai, M., Toyokuni, S., Hamanishi, J., Higuchi, T., Takakura, K., & Fujii, S. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1614 · Cited by 324 · see citing works
Crystal Structure of the Ectodomain of Human Transferrin Receptor
Lawrence, C. M., Ray, S., Babyonyshev, M., Galluser, R., Borhani, D. W., & Harrison, S. C. (1999) · Science · doi:10.1126/science.286.5440.779 · Cited by 315 · see citing works
Palei, P., & Rajesh, U. (2023) · Springer eBooks · doi:10.1007/978-3-031-24465-0_20 · Cited by 310 · see citing works
Heme Oxygenase: Recent Advances in Understanding Its Regulation and Role
Elbirt, K. K., & Bonkovsky, H. L. (1999) · Proceedings of the Association of American Physicians · doi:10.1111/paa.1999.111.5.438 · Cited by 306 · see citing works
Vinatier, D., Orazi, G., Cosson, M., & Dufour, P. (2001) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(00)00405-x · Cited by 299 · see citing works
George, J. N., & Raskob, G. E. (1998) · PubMed · Cited by 297 · 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
Oxidative stress may be a piece in the endometriosis puzzle.
Szczepańska, M., Koźlik, J., Skrzypczak, J., & Mikołajczyk, M. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00266-8 · Cited by 269 · see citing works
Inorganic Biochemistry of Iron Metabolism: From Molecular Mechanisms to Clinical Consequences
Crichton, R. R. (2001) · Cited by 244 · see citing works
Zweier, J. L., Broderick, R., Kuppusamy, P., Thompson-Gorman, S. L., & Lutty, G. A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)51062-6 · Cited by 244 · see citing works
Antiangiogenic Agents Are Effective Inhibitors of Endometriosis
Hull, M. L., Jones, D. S., Chan, C. L. K., Bruner‐Tran, K. L., Osteen, K. G., Tom, B. D. M., Fan, T. D., & Smith, S. K. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021912 · Cited by 243 · see citing works
Wagener, F. A. D. T. G., Feldman, E., de Witte, T., & Abraham, N. G. (1997) · Experimental Biology and Medicine · doi:10.3181/00379727-216-44197 · Cited by 241 · see citing works
Role of oxidative stress in endometriosis
Gupta, S., Agarwal, A., Krajcir, N., & Alvarez, J. G. (2006) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)62026-3 · Cited by 240 · see citing works
Antiangiogenesis Therapy for Endometriosis
Nap, A. W., Griffioen, A. W., Dunselman, G. A. J., Steege, J. C. A. B.-T., Thijssen, V. L., Evers, J. L. H., & Groothuis, P. G. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031406 · Cited by 239 · see citing works
Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons
D'Hooghe, T. M. (2002) · Human Reproduction Update · doi:10.1093/humupd/8.1.84 · Cited by 231 · see citing works
Molecular mechanisms involved in intestinal iron absorption
Sharp, P. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i35.4716 · Cited by 205 · see citing works
Cerebrovascular Inflammation Following Subarachnoid Hemorrhage
Sercombe, R., Dinh, Y. R. T., & Gomis, P. (2002) · The Japanese Journal of Pharmacology · doi:10.1254/jjp.88.227 · Cited by 203 · see citing works
Kunz, G., & LEYENDECKER, G. (2002) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(12)60108-4 · Cited by 201 · see citing works
The peritoneal environment in endometriosis
Oral, E. (1996) · Human Reproduction Update · doi:10.1093/humupd/2.5.385 · Cited by 201 · see citing works
Oxidative stress and endometriosis
Jackson, L. W., Schisterman, E. F., Dey-Rao, R., Browne, R. W., & Armstrong, D. (2005) · Human Reproduction · doi:10.1093/humrep/dei001 · Cited by 192 · see citing works
Vascular development in endometriosis
Groothuis, P. G., Nap, A. W., Winterhager, E., & Grümmer, R. (2005) · Angiogenesis · doi:10.1007/s10456-005-9005-x · Cited by 183 · see citing works
Laschke, M. W., & Menger, M. D. (2007) · Human Reproduction Update · doi:10.1093/humupd/dmm006 · Cited by 177 · 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
Potts, M. B., Koh, S.-E., Whetstone, W. D., Walker, B. A., Yoneyama, T., Claus, C. P., Manvelyan, H. M., & Noble-Haeusslein, L. J. (2006) · NeuroRX · doi:10.1016/j.nurx.2006.01.006 · Cited by 164 · see citing works
Role of alcohol in the regulation of iron metabolism
Harrison-Findik, D. D. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i37.4925 · Cited by 156 · see citing works
Nuclear factor-kappa B is constitutively activated in peritoneal endometriosis
González-Ramos, R., Donnez, J., Defrère, S., Leclercq, I. A., Squifflet, J. P., Lousse, J., & Langendonckt, A. V. (2007) · Molecular Human Reproduction · doi:10.1093/molehr/gam033 · Cited by 154 · see citing works
Self-citationTransition metal ion‐catalyzed oxygen activation during pathogenic processes
Hippeli, S., & Elstner, E. F. (1999) · FEBS Letters · doi:10.1016/s0014-5793(98)01665-2 · Cited by 153 · see citing works
Levy, A. P., Levy, J. E., Kalet-Litman, S., Miller‐Lotan, R., Levy, N. S., Asaf, R., Guetta, J., Yang, C., Purushothaman, K., Fuster, V., et al. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000251020.24399.a2 · Cited by 152 · 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
Self-citationGuo, S. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000096047 · Cited by 140 · see citing works
Iron overload in the peritoneal cavity of women with pelvic endometriosis
Van Langendonckt, A., Casanas-Roux, F., & Donnez, J. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03346-0 · Cited by 137 · see citing works
Self-citationMontagna, P., Capellino, S., Villaggio, B., Remorgida, V., Ragni, N., Cutolo, M., & Ferrero, S. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.11.200 · Cited by 135 · see citing works
Moura, E., Noordermeer, M. A., Verhoeven‐Duif, N. M., Verheul, A. F. M., & Marx, J. J. M. (1998) · Blood · doi:10.1182/blood.v92.7.2511 · Cited by 129 · see citing works
Therapeutic Effect of Angiostatin Gene Transfer in a Murine Model of Endometriosis
Dabrosin, C., Gyorffy, S., Margetts, P. J., Ross, C. A., & Gauldie, J. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64251-4 · Cited by 128 · see citing works
Early-stage endometriosis: adhesion and growth of human menstrual endometrium in nude mice
Nisolle, M., Casanas‐Roux, F., & Donnez, J. (2000) · Fertility and Sterility · doi:10.1016/s0015-0282(00)00601-4 · Cited by 128 · see citing works
Self-citationIron metabolism in the erythrophagocytosing Kupffer cell
Kondo, H. G., Saito, K., Grasso, J. P., & Aisen, P. (1988) · Hepatology · doi:10.1002/hep.1840080108 · Cited by 125 · see citing works
Iron Metabolism in Eukaryotes—Mars and Venus at It Again
Kaplan, J., & O’Halloran, T. V. (1996) · Science · doi:10.1126/science.271.5255.1510 · Cited by 124 · see citing works
Richardson, D. R. (2005) · Current Medicinal Chemistry · doi:10.2174/092986705774462996 · Cited by 123 · 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
Iron Chelator Research: Past, Present, and Future
Tam, T. F., Leung-Toung, R., Li, W., Wang, Y., Karimian, K., & Spino, M. (2003) · Current Medicinal Chemistry · doi:10.2174/0929867033457593 · Cited by 117 · see citing works
Macrophages, Oxidation, and Endometriosis
Santanam, N., Murphy, A. A., & Parthasarathy, S. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02779.x · Cited by 116 · see citing works
Defrère, S., Langendonckt, A. V., Vaesen, S., Jouret, M., Ramos, R., González, D., & Donnez, J. (2006) · Human Reproduction · doi:10.1093/humrep/del261 · Cited by 109 · see citing works
Self-citationIRON AND PROTEIN KINETICS STUDIED BY MEANS OF DOUBLY LABELED HUMAN CRYSTALLINE TRANSFERRIN*
Katz, J. H. (1961) · Journal of Clinical Investigation · doi:10.1172/jci104440 · Cited by 108 · see citing works
Garby, L., & Noyes, W. D. (1959) · Journal of Clinical Investigation · doi:10.1172/jci103925 · Cited by 107 · see citing works
Lousse, J., Langendonckt, A. V., González-Ramos, R., Defrère, S., Renkin, E., & Donnez, J. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.06.015 · Cited by 106 · see citing works
Self-citationSalamanca, A., & Beltrán, E. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57680-8 · Cited by 106 · see citing works
Menstrual 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
Barbieri, R. L. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00189-7 · Cited by 92 · see citing works
Potential involvement of hemoglobin and heme in the pathogenesis of peritoneal endometriosis
Van Langendonckt, A., Casanas-Roux, F., Dolmans, M.-M., & Donnez, J. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(01)03211-3 · Cited by 91 · see citing works
Self-citationSpectral and other studies on the intestinal haem receptor of the pig
Gräsbeck, R., Majuri, R., Kouvonen, I., & Tenhunen, R. (1982) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(82)90089-9 · Cited by 89 · see citing works
De novo formation of adhesions in endometriosis: the role of iron and free radical reactions
Arumugam, K., & Dip, Y. C. Y. (1995) · Fertility and Sterility · doi:10.1016/s0015-0282(16)57655-9 · Cited by 84 · see citing works
Nap, A. W., Dunselman, G. A. J., Griffioen, A. W., Mayo, K. H., Evers, J. L. H., & Groothuis, P. G. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.06.080 · Cited by 82 · see citing works
Receptor-mediated transport of heme by hemopexin regulates gene expression in mammalian cells
Alam, J., & Smith, A. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)84616-1 · Cited by 80 · see citing works
Sharpe-Timms, K. L., Zimmer, R. L., Ricke, E. A., Piva, M. A., & Horowitz, G. M. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03317-4 · Cited by 77 · see citing works
Iron metabolism in reticuloendothelial cells.
Deiss, A. (1983) · PubMed · Cited by 75 · see citing works
Antiproliferative and Apoptotic Effects of Iron Chelators on Human Cervical Carcinoma Cells
Simonart, T., Boelaert, J. R., Mosselmans, R., et al. (2002) · Gynecologic Oncology · doi:10.1006/gyno.2001.6570 · Cited by 70 · see citing works
Intracellular Labile Iron Modulates Adhesion of Human Monocytes to Human Endothelial Cells
Kartikasari, A. E. R., Georgiou, N., Visseren, F. L. J., Kats-Renaud, H. J. V., van Asbeck, B. S., & Marx, J. J. M. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000147406.00871.b3 · Cited by 66 · see citing works
Histologic confirmation of endometriosis in different peritoneal lesions
Moen, M. H., & Halvorsen, T. B. (1992) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349209021069 · Cited by 66 · see citing works
Donnez, J. (2002) · Human Reproduction Update · doi:10.1093/humupd/8.1.89 · Cited by 65 · see citing works
Self-citationFinch, C. A., Ragan, H. A., Dyer, I. A., et al. (1978) · Experimental Biology and Medicine · doi:10.3181/00379727-159-40343 · Cited by 63 · see citing works
Endometriotic Lesions Synthesize and Secrete a Haptoglobin-Like Protein1
Sharpe-Timms, K. L., Piva, M. A., Ricke, E. A., Surewicz, K. A., Zhang, Y. L., & Zimmer, R. L. (1998) · Biology of Reproduction · doi:10.1095/biolreprod58.4.988 · Cited by 61 · see citing works
Organochlorines and endometriosis: A mini-review
Heilier, J.-F., Donnez, J., & Lison, D. (2007) · Chemosphere · doi:10.1016/j.chemosphere.2007.09.044 · Cited by 60 · see citing works
Self-citationSharpe-Timms, K. L. (2000) · Human Reproduction · doi:10.1093/humrep/15.10.2180 · Cited by 59 · see citing works
Arumugam, K. (1994) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a138649 · Cited by 58 · see citing works
Brard, L., Granai, C. O., & Swamy, N. (2005) · Gynecologic Oncology · doi:10.1016/j.ygyno.2005.07.129 · Cited by 57 · see citing works
Iron requirements in erythropoietin therapy
Eschbach, J. W. (2005) · Best Practice & Research Clinical Haematology · doi:10.1016/j.beha.2004.09.005 · Cited by 57 · see citing works
Human macrophage hemoglobin‐iron metabolism in vitro
Custer, G., Balcerzak, S. P., & Rinehart, J. J. (1982) · American Journal of Hematology · doi:10.1002/ajh.2830130105 · Cited by 57 · see citing works
Piva, M. A., Horowitz, G. M., & Sharpe-Timms, K. L. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.6.7613 · Cited by 57 · see citing works
The Physiopathology of Endometriosis: Pollution and Dioxin
Koninckx, P. R. (1999) · Gynecologic and Obstetric Investigation · doi:10.1159/000052859 · Cited by 56 · see citing works
Haemoglobin expression in human endometrium
Dassen, H. H. N. M., Kamps, R., Punyadeera, C., Dijcks, F. A., de Goeij, A. F. P. M., EDERVEEN, A. G. H., Dunselman, G. A. J., & Groothuis, P. G. (2008) · Human Reproduction · doi:10.1093/humrep/dem430 · Cited by 56 · see citing works
Menstrual effluent induces epithelial-mesenchymal transitions in mesothelial cells
DEMİR, A. (2003) · Human Reproduction · doi:10.1093/humrep/deh042 · Cited by 51 · see citing works
Characterization of iron deposition in endometriotic lesions induced in the nude mouse model
Langendonckt, A. V. (2004) · Human Reproduction · doi:10.1093/humrep/deh182 · Cited by 50 · see citing works
The 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
Transplantation of cultured explants of human endometrium into nude mice
Nisolle, M., Casanas‐Roux, F., Marbaix, É., Jadoul, P., & Donnez, J. (2000) · Human Reproduction · doi:10.1093/humrep/15.3.572 · Cited by 43 · see citing works
Self-citationEndometriosis : current understanding and management
Shaw, R. W. (1995) · Medical Entomology and Zoology · Cited by 41 · see citing works
Cell Permeable Iron Chelators as Potential Cancer Chemotherapeutic Agents
Pahl, P. M. B., & Horwitz, L. D. (2005) · Cancer Investigation · doi:10.1080/07357900500359976 · Cited by 40 · see citing works
The endometrium and hormonal contraceptives
Benagiano, G., Pera, A., & Primiero, F. M. (2000) · Human Reproduction · doi:10.1093/humrep/15.suppl_1.101 · Cited by 39 · see citing works
Inflammatory leukocytes and iron turnover in experimental hemorrhagic lung trauma
Gorbunov, N. V., Asher, L. V. S., Ayyagari, V. N., & Atkins, J. L. (2005) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2005.06.007 · Cited by 39 · see citing works
Levels of Transferrin and Alpha 2-HS Glycoprotein in Women with and without Endometriosis
MATHUR, S. P., Lee, J. H., Jiang, H., Arnaud, P., & Rust, P. F. (1999) · Autoimmunity · doi:10.3109/08916939908995381 · Cited by 39 · see citing works
Chemical Assay of Iron in Ovarian Cysts: A New Diagnostic Method to Evaluate Endometriotic Cysts
Iizuka, M., Igarashi, M., Abe, Y., Ibuki, Y., Koyasu, Y., & Ikuma, K. (1998) · Gynecologic and Obstetric Investigation · doi:10.1159/000009999 · Cited by 37 · see citing works
Magnetic resonance relaxation time in evaluating the cyst fluid characteristics of endometrioma
Takahashi, K., Okada, S., Okada, M., Kitao, M., Kaji, Y., & Sugimura, K. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019266 · Cited by 36 · see citing works
The influence of iron homoeostasis on macrophage function
Ward, R. J., Wilmet, S., Legssyer, R., & Crichton, R. R. (2002) · Biochemical Society Transactions · doi:10.1042/bst0300762 · Cited by 35 · see citing works
Cytologic Diagnosis of Peritoneal Fluids
Stowell, S. B., Wiley, C. M., Perez‐Reyes, N., & Powers, C. N. (1997) · Acta Cytologica · doi:10.1159/000332709 · Cited by 34 · see citing works
Peritoneal endometriotic lesions differentially express a haptoglobin-like gene*
Piva, M. A. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.1.71 · Cited by 34 · see citing works
Martínez‐Román, S., Balasch, J., Creus, M. T., Fábregues, F., Carmona, F., Vilella, R., & Vanrell, J. A. (1997) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1997.tb00320.x · Cited by 32 · see citing works
Peritoneal endometriosis. Report of a case with cytologic, cytochemical and histopathologic study.
Gaulier, A., Jouret‐Mourin, A., & Marsan, C. (1983) · PubMed · Cited by 32 · see citing works
Hemopexin-dependent down-regulation of expression of the human transferrin receptor.
Taketani, S., Kohno, H., Sawamura, T., & Tokunaga, R. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)77445-0 · Cited by 29 · see citing works
The value of magnetic resonance relaxation time in staging ovarian endometrial cysts
Sugimura, K., Takemori, M., Sugiura, M., Okizuka, H., Kono, M., & Ishida, T. (1992) · British Journal of Radiology · doi:10.1259/0007-1285-65-774-502 · Cited by 25 · see citing works
Monocyte transferrin‐iron uptake in hereditary hemochromatosis
Sizemore, D. J., & Bassett, M. L. (1984) · American Journal of Hematology · doi:10.1002/ajh.2830160405 · Cited by 24 · see citing works
Iron mobilization from cultured rat bone marrow macrophages
Rama, R., Sánchez, J. L. M., & Octave, J. (1988) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/0167-4889(88)90043-2 · Cited by 19 · see citing works
Mobilisation of Iron from Peritoneal Rat Macrophages by Desferrioxamine
Kleber, E. E., Torrance, J. D., Bothwell, T. H., et al. (1981) · Scandinavian Journal of Haematology · doi:10.1111/j.1600-0609.1981.tb00474.x · Cited by 18 · see citing works
Defrère, S., Donnez, J., Moulin, P., Befahy, P., González-Ramos, R., Lousse, J., & Langendonckt, A. V. (2007) · Gynecologic and Obstetric Investigation · doi:10.1159/000110350 · Cited by 14 · see citing works
Self-citationExpression of inducible heme oxygenase in human endometrium
Casanas‐Roux, F., Langendonckt, A. V., Dolmans, M., & Donnez, J. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)04395-9 · Cited by 11 · see citing works
Self-citationIdentification of transferrin receptor in cervical and endometrial tissues
Mizuuchi, H., Kudo, R., Tamura, H., et al. (1988) · Gynecologic Oncology · doi:10.1016/s0090-8258(88)80007-6 · Cited by 10 · see citing works
[Ferritin levels in the peritoneal fluid--a new endometriosis marker?].
Polak, G., Wertel, I., Tarkowski, R., Morawska, D., Nowakowski, A. M., & Kotarski, J. (2006) · PubMed · Cited by 7 · see citing works
[The effect of iron on peritoneal macrophage activity and sperm phagocytosis in rats].
Skowron, J. (2000) · PubMed · Cited by 6 · see citing works
[Asymptomatic peritoneal endometriosis following cesarean section].
Petrozza, V., M, M. F., Pulvirenti, S., Massimi, G., De Salazar, C., & Carpino, F. (1993) · PubMed · Cited by 5 · see citing works
[Peritoneal environment in endometriosis].
Koga, K. A., Osuga, Y., & Taketani, Y. (2001) · PubMed · Cited by 5 · see citing works
Beale, S. I., & Yeh, J. I. (1999) · Nature Structural Biology · doi:10.1038/13264 · Cited by 5 · see citing works
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Cited by
Sorted by citations
Endometriosis: pathogenesis and treatment
Vercellini, P., Viganò, P., Somigliana, E., & Fedele, L. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.255 · Cited by 1,940 · see citing works
Smolarz, B., Szyłło, K., & Romanowicz, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910554 · Cited by 560 · see citing works
Bacci, M., Capobianco, A., Monno, A., Cottone, L., Di Puppo, F., Camisa, B., Mariani, M., Brignole, C., Ponzoni, M., Ferrari, S., et al. (2009) · The American Journal of Pathology · doi:10.2353/ajpath.2009.081011 · Cited by 458 · see citing works
Oxidative Stress and Endometriosis: A Systematic Review of the Literature
Scutiero, G., Iannone, P., Bernardi, G., Bonaccorsi, G., Spadaro, S., Volta, C. A., Greco, P., & Nappi, L. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/7265238 · Cited by 436 · see citing works
Oxidative stress in the pelvic cavity and its role in the pathogenesis of endometriosis
Donnez, J., Binda, M. M., Donnez, O., & Dolmans, M.-M. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.07.1075 · Cited by 251 · see citing works
Self-citationPathogenetic 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
Involvement of the nuclear factor-κB pathway in the pathogenesis of endometriosis
González-Ramos, R., Van Langendonckt, A., Defrère, S., Lousse, J.-C., Colette, S., Devoto, L., & Donnez, J. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.01.013 · Cited by 179 · see citing works
Self-citationDing, D., Liu, X., Duan, J., & Guo, S.-W. (2015) · Human Reproduction · doi:10.1093/humrep/dev025 · Cited by 139 · see citing works
Can Endometriosis-Related Oxidative Stress Pave the Way for New Treatment Targets?
Cacciottola, L., Donnez, J., & Dolmans, M.-M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22137138 · Cited by 118 · see citing works
Self-citationCancer-associated mutations in endometriosis: shedding light on the pathogenesis and pathophysiology
Guo, S.-W. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmz047 · Cited by 96 · see citing works
Guo, S.-W., Ding, D., Shen, M., & Liu, X. (2015) · Reproductive Sciences · doi:10.1177/1933719115570907 · Cited by 86 · see citing works
Goud, P. T., Bai, D., & Abu-Soud, H. M. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.51811 · Cited by 88 · see citing works
Maitra, D., Shaeib, F., Abdulhamid, I., Abdulridha, R. M., Saed, G. M., Diamond, M. P., Pennathur, S., & Abu-Soud, H. M. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.04.009 · Cited by 64 · see citing works
Mechanism of Hypochlorous Acid-Mediated Heme Destruction and Free Iron Release
Maitra, D., Byun, J., Andreana, P. R., Abdulhamid, I., Saed, G. M., Diamond, M. P., Pennathur, S., & Abu-Soud, H. M. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.03.040 · Cited by 51 · see citing works
Polak, G., Barczyński, B., Wertel, I., Kwaśniewski, W., Bednarek, W., Derewianka-Polak, M., Frąszczak, K., Olajossy, M., & Kotarski, J. (2018) · Annals of Agricultural and Environmental Medicine · doi:10.26444/aaem/75802 · Cited by 41 · see citing works
Yang, H., Zhu, L., Wang, S., Lang, J., & Xu, T. (2015) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2013.06.003 · Cited by 37 · see citing works
Reduced hemopexin levels in peritoneal fluid of patients with endometriosis
Wölfler, M. M., Meinhold-Heerlein, I. M., Henkel, C., Rath, W., Neulen, J., Maass, N., & Bräutigam, K. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.05.010 · Cited by 35 · see citing works
Smolarz, B., Szaflik, T., Romanowicz, H., & Szyłło, K. (2020) · Disease Markers · doi:10.1155/2020/8845704 · Cited by 27 · see citing works
The Double Engines and Single Checkpoint Theory of Endometriosis
Hsu, C.-F., Khine, A. A., Huang, H.-S., & Chu, T.-Y. (2022) · Biomedicines · doi:10.3390/biomedicines10061403 · Cited by 12 · see citing works
An Analysis of <i>ESR2</i> and <i>CYP19A1</i> Gene Expression Levels in Women With Endometriosis
SZAFLIK, T., SMOLARZ, B., MROCZKOWSKA, B., KULIG, B., SOJA, M., ROMANOWICZ, H., BRYŚ, M., FORMA, E., & SZYŁŁO, K. (2020) · In Vivo · doi:10.21873/invivo.11970 · Cited by 11 · 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
Self-citationAssociation between single nucleotide polymorphism of the CYP19A1 and ESR2 genes and endometriosis
Smolarz, B., & Romanowicz, H. (2021) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-021-06051-5 · Cited by 7 · see citing works
- Authors
- Defrere, S., Lousse, J. C., Gonzalez-Ramos, R., Colette, S., Donnez, J., & Van Langendonckt, A.
- Affiliations
- Cliniques Universitaires Saint-Luc (BE)
- ORCID
- Donnez, J.
- Venue
- Molecular Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2008-05-28
- Volume
- 14
- Issue
- 7
- Pages
- 377-385
- ISSN
- 1360-9947 (ISSN-L)
- 1460-2407
- OpenAlex
- W2119501943
- Cited by
- 204
- References
- 127
- Citations by year
- 2026: 14 · 2025: 26 · 2024: 20 · 2023: 18 · 2022: 15 · 2021: 12 · 2020: 10 · 2019: 7 · 2018: 4 · 2017: 8 · 2016: 9 · 2015: 10 · 2014: 7 · 2013: 9 · 2012: 13
- FWCI
- 1.02
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Libraries (submittedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, iron overload, peritoneal endometriosis, peritoneal macrophages, peritoneal fluid, retrograde menstruation, oxidative stress, iron chelation, iron metabolism, pathogenesis
- MeSH terms
- Animals, Endometriosis, Female, Humans, Iron, Models, Biological, Peritoneum, Oxidative Stress, Iron Overload
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