The DOI matches its Crossref record; 71 of the 71 references it cites were found in a registry or an index.
Oxidative stress in the pelvic cavity and its role in the pathogenesis of endometriosis
Open accessAbstract
Endometriosis is a disorder associated with a general inflammatory response in the peritoneal cavity. Oxidative stress is a potential factor involved in the pathophysiology of this disease, and reactive oxygen species (ROS) are implicated in this process. Indeed, in healthy individuals, ROS and antioxidants are in balance, but when balance is tipped toward an overabundance of ROS, oxidative stress occurs and can impact the entire reproductive lifespan of a woman. Reactive oxygen species are intermediaries produced by normal oxygen metabolism but are known to have deleterious effects. Excessive release of ROS induces cellular damage and alters cellular function by regulating protein activity and gene expression, leading to harmful effects. To protect themselves, cells have developed antioxidant systems to limit production of ROS, inactivate them, and repair cell damage. Understanding of the control of hemoglobin, heme, and iron-induced redox balance in endometriosis led us to propose a number of hypotheses to explain why oxidative stress is induced in case of pelvic endometriosis. Erythrocytes, apoptotic endometrial tissue, and cell debris transplanted into the peritoneal cavity by menstrual reflux and macrophages have all been cited as potential inducers of oxidative stress. Erythrocytes are likely to release pro-oxidant and proinflammatory factors, such as hemoglobin and its highly toxic by-products heme and iron, into the peritoneal environment. Iron and heme are essential to living cells, but unless appropriately chelated, free iron, and to a lesser extent heme, play a key role in the formation of deleterious ROS.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“First, the oxidative stress in the uterus during menstruation and in the peritoneal cavity following retrograde menstruation (248) are recognized as potential causative factors to induce genetic or epigenetic changes.”
From Pathogenesis of endometriosis: The genetic/epigenetic theory (2019) · cites this paper as [248]
In the citing paper
“Retrograde menstruation and bleeding of endometriotic lesions are responsible for the presence of erythrocytes in the pelvic cavity, which are likely to release pro-oxidant and proinflammatory factors like hemoglobin and its highly toxic byproducts heme and iron [27,28,29,30].”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [30]
In the citing paper
“Of course, suppressing ovulation and reducing the amount of menstrual bleeding greatly reduces the number of erythrocytes regurgitated into the pelvis, resulting in a decrease in oxidative stress and the inflammatory environment [30].”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [30]
In the citing paper
“By inducing amenorrhea and halting menstrual bleeding and reflux, or even simply lessening its severity, pelvic oxidative stress, the main source of inflammation, can be significantly reduced [30].”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [30]
In the citing paper
“Retrograde menstruation and bleeding in endometriosis lesions generate an iron overload and oxidative stress in the peritoneal cavity (109) and/or in the endometriosis tissue (110).”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [109]
Citations
Cites
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166
The rise of oxygen in Earth's early ocean and atmosphere
Lyons, T. W., Reinhard, C. T., & Planavsky, N. J. (2014) · Nature · doi:10.1038/nature13068 · Cited by 2,810
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334
Oxidative stress as a mediator of apoptosis
Buttke, T. M., & Sandstrom, P. A. (1994) · Immunology Today · doi:10.1016/0167-5699(94)90018-3 · Cited by 2,149
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772
Role of oxidative stress in female reproduction
Agarwal, A., Gupta, S., & Sharma, R. K. (2005) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-3-28 · Cited by 1,729
The effects of oxidative stress on female reproduction: a review
Agarwal, A. K., Aponte, A., Premkumar, B. J., Shaman, A. A., & Gupta, S. (2012) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-10-49 · Cited by 1,721
Nisolle, M., & Donnez, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00191-x · Cited by 1,279
Self-citationFerritin: 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
Endometriosis and infertility: pathophysiology and management
de Ziegler, D., Borghese, B., & Chapron, C. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60490-4 · Cited by 853
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
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
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
Self-citationOxidative 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
Self-citationRedox-optimized ROS balance: A unifying hypothesis
Aon, M. A., Cortassa, S. C., & O'Rourke, B. P. (2010) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2010.02.016 · Cited by 381
Oxidative stress and antioxidants: exposure and impact on female fertility
Ruder, E. H., Hartman, T. J., Blumberg, J., & Goldman, M. B. (2008) · Human Reproduction Update · doi:10.1093/humupd/dmn011 · Cited by 351
Reactive Oxygen Species Controls Endometriosis Progression
Ngô, C., Chéreau, C., Nicco, C., Weill, B., Chapron, C., & Batteux, F. (2009) · The American Journal of Pathology · doi:10.2353/ajpath.2009.080804 · Cited by 292
Gut Ischemia, Oxidative Stress, and Bacterial Translocation in Elevated Abdominal Pressure in Rats
Eleftheriadis, E., Kotzampassi, K. E., Papanotas, K., Heliadis, N., & Sarris, K. (1996) · World Journal of Surgery · doi:10.1007/s002689900002 · Cited by 274
Yamawaki, H., Pan, S., Lee, R. T., & Berk, B. C. (2005) · Journal of Clinical Investigation · doi:10.1172/jci200523001 · Cited by 252
Yamawaki, H., Pan, S., Lee, R. T., et al. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23001 · Cited by 216
Potential 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
Self-citationKinase signalling pathways in endometriosis: potential targets for non-hormonal therapeutics
McKinnon, B. D., Kocbek, V., Nirgianakis, K., Bersinger, N. A., & Mueller, M. D. (2016) · Human Reproduction Update · doi:10.1093/humupd/dmv060 · Cited by 195
Angiongenesis: a new theory for endometriosis
Healy, D. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.736 · Cited by 173
Rout, U. K., Saed, G. M., & Diamond, M. P. (2005) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-3-1 · Cited by 171
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
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
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 152
Self-citationKokorine, 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
Self-citationImpact of ovarian endometrioma on assisted reproduction outcomes
Gupta, S., Agarwal, A. K., Agarwal, R., & de Mola, J. R. L. (2006) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)61439-3 · Cited by 148
Santulli, P., Chouzenoux, S., Fiorese, M., Marcellin, L., Lemaréchal, H., Millischer, A., Batteux, F., Borderie, D., & Chapron, C. (2014) · Human Reproduction · doi:10.1093/humrep/deu290 · Cited by 144
Guo, S. (2006) · Gynecologic and Obstetric Investigation · doi:10.1159/000096047 · Cited by 141
Localization of laminin, fibronectin, E-cadherin, and integrins in endometrium and endometriosis
Béliard, A., Donnez, J., Nisolle, M., & Foidart, J. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81909-7 · Cited by 141
Self-citationOxidative stress biomarkers in patients with endometriosis: systematic review
Carvalho, L. F. P., Samadder, A. N., Agarwal, A., Fernandes, L. F. C., & Abrão, M. S. (2012) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-012-2439-7 · Cited by 140
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
Self-citationPeritoneal endometriosis is an inflammatory disease.
Lousse, J., van Langendonckt, A., Defrère, S., Ramos, R. G., Colette, S., & Donnez, J. (2012) · Frontiers in Bioscience · doi:10.2741/358 · Cited by 137
Lousse, J., Defrère, S., Langendonckt, A. V., Gras, J. M., González-Ramos, R., Colette, S., & Donnez, J. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.02.103 · Cited by 137
Self-citationMolinas, C. R., Mynbaev, O. A., Pauwels, A., Novák, P., & Koninckx, P. R. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01964-1 · Cited by 134
Oxidative Stress and Antioxidant Defense in Endometriosis and Its Malignant Transformation
Iwabuchi, T., Yoshimoto, C., Shigetomi, H., & Kobayashi, H. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/848595 · Cited by 129
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
Self-citationPeritoneal endometriosis is an inflammatory disease
Donnez, J. (2012) · Frontiers in Bioscience · doi:10.2741/e358 · Cited by 127
Self-citationMeasurable serum markers of oxidative stress response in women with endometriosis
Lambrinoudaki, I. V., Augoulea, A., Christodoulakos, G., Economou, E. V., Kaparos, G., Kontoravdis, A., Papadias, C. B., & Creatsas, G. C. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.11.021 · Cited by 124
The mTOR/AKT Inhibitor Temsirolimus Prevents Deep Infiltrating Endometriosis in Mice
Leconte, M., Nicco, C., Ngô, C., Chéreau, C., Chouzenoux, S., Marut, W., Guibourdenche, J., Arkwright, S., Weill, B. J., Chapron, C., et al. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.04.020 · Cited by 117
Endometriosis: A Disease of Oxidative Stress?
Murphy, A. A., Santanam, N., & Parthasarathy, S. (1998) · Seminars in Reproductive Medicine · doi:10.1055/s-2007-1016286 · Cited by 116
Is endometriosis an endometrial disease?
Vinatier, D., Cosson, M., & Dufour, P. (2000) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(99)00263-8 · Cited by 115
Donnez, J., Donnez, O., Orellana, R., Binda, M. M., & Dolmans, M. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.01.019 · Cited by 112
Self-citationProtective role of heme oxygenase-1 induction in carbon tetrachloride-induced hepatotoxicity
Nakahira, K., Takahashi, T., Shimizu, H., Maeshima, K., Uehara, K., Fujii, H., Nakatsuka, H., Yokoyama, M., Akagi, R., & Morita, K. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(03)00444-1 · Cited by 111
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
Self-citationLousse, 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 107
Self-citationReactive oxygen species and adhesion formation: Clinical implications in adhesion prevention
Binda, M. M. (2003) · Human Reproduction · doi:10.1093/humrep/deg481 · Cited by 101
Self-citationSomigliana, E., Vigand, P., Gaffuri, B., Guarneri, D., Busacca, M., & Vignali, M. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019353 · Cited by 100
Surgical stress and the small intestine: Role of oxygen free radicals
Anup, R., Aparna, V., Pulimood, A. B., & Balasubramanian, K. A. (1999) · Surgery · doi:10.1016/s0039-6060(99)70209-6 · Cited by 96
Targeting oxidative stress to treat endometriosis
Harlev, A., Gupta, S., & Agarwal, A. K. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2015.1077226 · Cited by 92
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
Self-citationSillem, M. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.730 · Cited by 86
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
Elkelani, O. A., Binda, M. M., Molinas, C. R., & Koninckx, P. R. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.07.933 · Cited by 68
Self-citationDonnez, J., Nisolle, M., Casanas-Roux, F., Brion, P., & DaFerreira, N. C. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019024 · Cited by 65
Self-citationThree-dimensional architectures of peritoneal endometriosis
Donnez, J., Nisolle, M., & Casanas‐Roux, F. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55012-2 · Cited by 60
Self-citationComparison of Peritoneal Oxidative Stress During Laparoscopy and Laparotomy
de Souza, Â. M. B., Rogers, M. S., Wang, C. C., Yuen, P. M., & Ng, P. S. (2003) · The Journal of the American Association of Gynecologic Laparoscopists · doi:10.1016/s1074-3804(05)60237-x · Cited by 60
Taşkın, Ö., Buhur, A., Birincioğlu, M., Burak, F., Atmaca, R., Yılmaz, İ., & Wheeler, J. (1998) · The Journal of the American Association of Gynecologic Laparoscopists · doi:10.1016/s1074-3804(98)80078-9 · Cited by 60
Oxygen toxicity: an introduction.
Cc, B. (1989) · PubMed · Cited by 53
Expression of eicosanoid biosynthetic and catabolic enzymes in peritoneal endometriosis
Lousse, J. C., Defrère, S., Colette, S., Langendonckt, A. V., & Donnez, J. (2009) · Human Reproduction · doi:10.1093/humrep/dep408 · Cited by 52
Self-citationCharacterization 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
Menstruum Induces Changes in Mesothelial Cell Morphology
Koks, C. A. M., Demir-Weusten, A. Y., Groothuis, P. G., Dunselman, G. A. J., de Goeij, A. F. P. M., & Evers, J. L. H. (2000) · Gynecologic and Obstetric Investigation · doi:10.1159/000010271 · Cited by 44
Kerr, R. A. (2005) · Science · doi:10.1126/science.308.5729.1730 · Cited by 40
Lindahl, S. G. E. (2008) · Anesthesiology · doi:10.1097/aln.0b013e31817b5a7e · Cited by 31
Implantation defect in endometriosis: endometrium or peritoneal fluid.
Selam, B., & Arici, A. M. (2000) · PubMed · Cited by 31
Microscopic endometriosis: impact on our understanding of the disease and its surgery
Koninckx, P. R., Donnez, J., & Brosens, I. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.10.038 · Cited by 22
Self-citationElkins, T. E., Warren, J. S., PORTZ, D. M., & McNeeley, S. G. (1991) · PubMed · Cited by 17
Endométriose et génétique : les gènes sont-ils responsables de la maladie ?
Borghese, B., Vaiman, D., de Ziegler, D., & Chapron, C. (2010) · Journal de gynécologie, obstétrique et biologie de la reproduction. Supplément/Journal de gynécologie obstétrique et biologie de la reproduction · doi:10.1016/j.jgyn.2010.03.006 · Cited by 15
Griffin, D. W. (2017) · CRC Press eBooks · doi:10.4324/9781351241496-13 · Cited by 5
Flagged first, then by citations
Cited by
Sorted by citations
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
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
Influence of follicular fluid and cumulus cells on oocyte quality: clinical implications
Broi, M. G. D., Giorgi, V. S. I., Wang, F., Keefe, D. L., Albertini, D. F., & Navarro, P. A. (2018) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-018-1143-3 · Cited by 314
Estrogen-progestins and progestins for the management of endometriosis
Vercellini, P., Buggio, L., Berlanda, N., Barbara, G., Somigliana, E., & Bosari, S. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.10.022 · Cited by 243
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
Metadata
- Authors
- Donnez, J., Binda, M. M., Donnez, O., & Dolmans, M.-M.
- Affiliations
- UCLouvain (BE)
- Cliniques Universitaires Saint-Luc (BE)
- Corresponding author
- Dolmans, Marie-Madeleine
- Venue
- Fertility and Sterility
- Publisher
- Elsevier BV
- Published
- 2016-10
- Volume
- 106
- Issue
- 5
- Pages
- 1011-1017
- ISSN
- 0015-0282 (ISSN-L)
- OpenAlex
- W2515189190
- Semantic Scholar
- 167a6e84e12265cafa8a82a56c2deaae1e4d2fc9
- Cited by
- 251
- References
- 71
- Citations by year
- 2026: 14 · 2025: 36 · 2024: 32 · 2023: 28 · 2022: 30 · 2021: 26 · 2020: 23 · 2019: 17 · 2018: 22 · 2017: 20 · 2016: 3
- FWCI
- 2.92
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Fertility and Sterility (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Libraries (submittedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Biochemistry (medical) › Antioxidant Activity and Oxidative Stress
- Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
- Keywords
- endometriosis, oxidative stress, reactive oxygen species, antioxidants, heme, iron, hemoglobin, erythrocytes, macrophages, peritonitis, redox homeostasis, pathogenesis
- MeSH terms
- Animals, Antioxidants, Endometriosis, Erythrocytes, Female, Hemoglobins, Humans, Iron, Macrophages, Peritoneal Cavity, Risk Factors, Biomarkers, Reactive Oxygen Species, Oxidative Stress, Inflammation Mediators
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