Oxidative Stress and Endometriosis: A Systematic Review of the Literature
Open accessAbstract
Endometriosis is one of the most common gynaecologic diseases in women of reproductive age. It is characterized by the presence of endometrial tissue outside the uterine cavity. The women affected suffer from pelvic pain and infertility. The complex etiology is still unclear and it is based on three main theories: retrograde menstruation, coelomic metaplasia, and induction theory. Genetics and epigenetics also play a role in the development of endometriosis. Recent studies have put the attention on the role of oxidative stress, defined as an imbalance between reactive oxygen species (ROS) and antioxidants, which may be implicated in the pathophysiology of endometriosis causing a general inflammatory response in the peritoneal cavity. Reactive oxygen species are intermediaries produced by normal oxygen metabolism and are inflammatory mediators known to modulate cell proliferation and to have deleterious effects. A systematic review was performed in order to clarify the different roles of oxidative stress and its role in the development of endometriosis. Several issues have been investigated: iron metabolism, oxidative stress markers (in the serum, peritoneal fluid, follicular fluid, peritoneal environment, ovarian cortex, and eutopic and ectopic endometrial tissue), genes involved in oxidative stress, endometriosis‐associated infertility, and cancer development.
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 pathogenesis of malignant transformation of endometriosis remains unelucidated; however, certain studies implicate oxidative stress according to a two-step process in endometriotic carcinogenesis.
“The pathogenesis of malignant transformation of endometriosis remains unelucidated; however, certain studies implicate oxidative stress according to a two-step process in endometriotic carcinogenesis [13].”
From Clear cell carcinoma arising from abdominal wall endometriosis—A report on two cases and literature review (2022) · cites this paper as [13]
In the second step of endometriotic carcinogenesis, cancer progression occurs due to antioxidant production which prolongs the survival of affected cell populations, thus promoting carcinogenesis.
“In the second step, cancer progression occurs due to antioxidant production which prolongs the survival of affected cell populations, thus promoting carcinogenesis [13, 14].”
From Clear cell carcinoma arising from abdominal wall endometriosis—A report on two cases and literature review (2022) · cites this paper as [13]
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
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 · see citing works
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 1,674 · see citing works
ESHRE guideline for the diagnosis and treatment of endometriosis
Kennedy, S., Bergqvist, A., Chapron, C., D’Hooghe, T., Dunselman, G., Greb, R., Hummelshoj, L., Prentice, A., & Saridogan, E. (2005) · Human Reproduction · doi:10.1093/humrep/dei135 · Cited by 1,584 · see citing works
(1927) · PubMed Central · Cited by 1,008 · see citing works
Pathogenic mechanisms in endometriosis-associated infertility
Gupta, S., Goldberg, J. M., Aziz, N., Goldberg, E., Krajcir, N., & Agarwal, A. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.02.093 · Cited by 409 · 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
Agarwal, A. K., Gupta, S., Sekhon, L. H., & Shah, R. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.1964 · Cited by 360 · 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
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 · 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
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
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 · see citing works
Singh, A., Chattopadhyay, R., Chakravarty, B., et al. (2013) · Reproductive Toxicology · doi:10.1016/j.reprotox.2013.08.005 · Cited by 196 · see citing works
EVIDENCE FOR THE RISK OF PELVIC ENDOMETRIOSIS BY AGE, RACE AND SOCIOECONOMIC STATUS1
Houston, D. E. (1984) · Epidemiologic Reviews · doi:10.1093/oxfordjournals.epirev.a036270 · Cited by 196 · 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
Prieto, L., Quesada‐Espinosa, J. F., Cambero, O., Pacheco, A., Pellicer, A., Codoceo, R., & García-Velasco, J. A. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.03.052 · Cited by 190 · see citing works
Aspectos epidemiológicos e clínicos da endometriose pélvica: uma série de casos
Bellelis, P., Dias, J., Podgaec, S., Gonzales, M., Baracat, E. C., & Abrão, M. S. (2010) · Revista da Associação Médica Brasileira · doi:10.1590/s0104-42302010000400022 · Cited by 166 · see citing works
Kennedy, S., Mardon, H., & Barlow, D. (1995) · Journal of Assisted Reproduction and Genetics · doi:10.1007/bf02214126 · Cited by 157 · see citing works
Pathogenesis of endometriosis: the role of genetics, inflammation and oxidative stress
Augoulea, A., Alexandrou, A. P., Creatsa, M. G., Vrachnis, N., & Lambrinoudaki, I. V. (2012) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-012-2357-8 · Cited by 140 · see citing works
Oxidative 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 · see citing works
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 139 · see citing works
Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis.
Matsuzaki, S., & Schubert, B. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.08.068 · Cited by 138 · see citing works
Peritoneal 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 · see citing works
Endometriosis: New concepts in the pathogenesis
Signorile, P. G., & Baldi, A. (2010) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2010.03.008 · Cited by 136 · see citing works
Pathogenesis of endometriosis: The role of defective ‘immunosurveillance’
Christodoulakos, G., Augoulea, A., Lambrinoudaki, I., Sioulas, V., & Creatsas, G. (2007) · The European Journal of Contraception & Reproductive Health Care · doi:10.1080/13625180701387266 · Cited by 133 · see citing works
The role of the oxidative-stress in the endometriosis-related infertility
Augoulea, A., Mastorakos, G., Lambrinoudaki, I., Christodoulakos, G., & Creatsas, G. (2009) · Gynecological Endocrinology · doi:10.1080/09513590802485012 · Cited by 129 · see citing works
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 128 · see citing works
Mier‐Cabrera, J., Jiménez-Zamudio, L. A., Garcı́a-Latorre, E., Cruz-Orozco, O., & Hernández‐Guerrero, C. (2010) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2010.02777.x · Cited by 127 · see citing works
Peritoneal endometriosis is an inflammatory disease
Donnez, J. (2012) · Frontiers in Bioscience · doi:10.2741/e358 · Cited by 127 · see citing works
Goud, P. T., Goud, A. P., Joshi, N., Puscheck, E. E., Diamond, M. P., & Abu‐Soud, H. M. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.03.053 · Cited by 126 · see citing works
Measurable 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 · see citing works
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 · see citing works
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 · see citing works
Verit, F. F., Erel, O., & Celik, N. (2007) · Human Reproduction · doi:10.1093/humrep/dem340 · Cited by 115 · see citing works
Mier‐Cabrera, J., Genera-García, M., la Jara-Díaz, J. F. D., Perichart‐Perera, O., Vadillo‐Ortega, F., & Hernández‐Guerrero, C. (2007) · International Journal of Gynecology & Obstetrics · doi:10.1016/j.ijgo.2007.08.018 · Cited by 111 · 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
Osborn, B. H., Haney, A. F., Misukonis, M. A., & Weinberg, J. B. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(01)02940-5 · Cited by 102 · see citing works
New insights into the pathophysiology of endometriosis: from chronic inflammation to danger signal
Kajihara, H., Yamada, Y., Kanayama, S., Furukawa, N., 野口, 武., Haruta, S., Yoshida, S., Sado, T., Oi, H., & Kobayashi, H. (2010) · Gynecological Endocrinology · doi:10.3109/09513590.2010.507292 · Cited by 96 · see citing works
Broi, M. D. D., & Navarro, P. (2016) · Cell and Tissue Research · doi:10.1007/s00441-015-2339-9 · Cited by 94 · see citing works
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 90 · see citing works
Oxidative Stress Statues in Serum and Follicular Fluid of Women with Endometriosis.
Nasiri, N., Moini, A., Eftekhari‐Yazdi, P., Karimian, L., Yazdi, R. S., & Arabipoor, A. (2017) · PubMed Central · doi:10.22074/cellj.2016.4724 · Cited by 81 · see citing works
Role of Oxidative Stress in Epigenetic Modification in Endometriosis
Ito, F., Yamada, Y., 重光, 愛., Akinishi, M., Kaniwa, H., Miyake, R., Yamanaka, S., & Kobayashi, H. (2017) · Reproductive Sciences · doi:10.1177/1933719117704909 · Cited by 79 · see citing works
Ngô, C., Nicco, C., Leconte, M., Chéreau, C., Arkwright, S., Vacher‐Lavenu, M., Weill, B., Chapron, C., & Batteux, F. (2010) · The Journal of Pathology · doi:10.1002/path.2756 · Cited by 78 · see citing works
(2013) · PubMed · Cited by 63 · see citing works
Ota, H., Igarashi, S., Hatazawa, J., & Tanaka, T. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81470-7 · Cited by 60 · see citing works
Oxidative Damage and Mitochondrial DNA Mutations with Endometriosis
Kao, S., HUANG, H., Hsieh, R., Chen, S., Tsai, M.-C., & Tzeng, C.-R. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1338.021 · Cited by 54 · see citing works
Redox-Active Iron-Induced Oxidative Stress in the Pathogenesis of Clear Cell Carcinoma of the Ovary
Yamada, Y., Shigetomi, H., Onogi, A., et al. (2011) · International Journal of Gynecological Cancer · doi:10.1097/igc.0b013e318222cfdd · Cited by 53 · see citing works
Potential scenarios leading to ovarian cancer arising from endometriosis
Kobayashi, H. (2015) · Redox Report · doi:10.1179/1351000215y.0000000038 · Cited by 52 · see citing works
Role of 8-iso-prostaglandin F2α and 25-hydroxycholesterol in the pathophysiology of endometriosis
Sharma, I., Dhaliwal, L., Saha, S. C., Sangwan, S., & Dhawan, V. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.01.141 · Cited by 51 · see citing works
Singh, N., Lata, K., Naha, M., et al. (2014) · Journal of Human Reproductive Sciences · doi:10.4103/0974-1208.138874 · Cited by 49 · see citing works
Indices of Oxidative Stress in Eutopic and Ectopic Endometria of Women with Endometriosis
Öner-İyidoğan, Y., Koçak, H., Gürdöl, F., Korkmaz, D., & Buyru, F. (2004) · Gynecologic and Obstetric Investigation · doi:10.1159/000076691 · Cited by 49 · see citing works
Türkyılmaz, E., Yıldırım, M., Çendek, B. D., Baran, P., Alışık, M., Dalgacı, A. F., & Yavuz, A. F. (2016) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2016.02.027 · Cited by 48 · see citing works
Hevir, N., Ribič-Pucelj, M., & Rižner, T. L. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2012.12.019 · Cited by 45 · see citing works
A potential link of oxidative stress and cell cycle regulation for development of endometriosis
Shigetomi, H., Higashiura, Y., Kajihara, H., & Kobayashi, H. (2012) · Gynecological Endocrinology · doi:10.3109/09513590.2012.683071 · Cited by 40 · see citing works
Redox regulation of microRNAs in endometriosis-associated pain
Wright, K. R., Mitchell, B. L., & Santanam, N. (2017) · Redox Biology · doi:10.1016/j.redox.2017.04.037 · Cited by 38 · 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
Increased oxidation-related glutathionylation and carbonic anhydrase activity in endometriosis
Andrisani, A., Donà, G., Brunati, A. M., Clari, G., Armanini, D., Ragazzi, E., Ambrosini, G., & Bordin, L. (2014) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2014.01.016 · Cited by 34 · see citing works
Measurement of oxidative stress in the follicular fluid of infertility patients with an endometrioma
Nakagawa, K., Hisano, M., Sugiyama, R., et al. (2015) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-015-3834-7 · Cited by 30 · see citing works
Andrade, S. S., Azevedo, A. D. C., Guerra, I. M., Paredes‐Gamero, E. J., Gonçalves, G., Bonetti, T. C., Albertoni, G., Schor, E., Barreto, J. A., Oliva, M. L. V., et al. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.01.034 · Cited by 30 · see citing works
Low-Density Lipoproteins Oxidation and Endometriosis
Polak, G., Barczyński, B., Kwaśniewski, W. M., Bednarek, W., Wertel, I., Derewianka-Polak, M., & Kotarski, J. (2013) · Mediators of Inflammation · doi:10.1155/2013/624540 · Cited by 29 · see citing works
Bragatto, F. B., Barbosa, C. P., Christofolini, D. M., Peluso, C., dos Santos, A. A., Mafra, F., Cavalcanti, V., Hix, S., & Bianco, B. A. V. (2013) · Reproductive Health · doi:10.1186/1742-4755-10-32 · Cited by 11 · see citing works
Zhu, X. H., Zhu, X., Zellweger, R., et al. (1995) · Shock · doi:10.1097/00024382-199506000-00045 · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Targeting Oxidative Stress Involved in Endometriosis and Its Pain
Clower, L., Fleshman, T., Geldenhuys, W. J., & Santanam, N. (2022) · Biomolecules · doi:10.3390/biom12081055 · Cited by 145 · see citing works
Liao, T.-L., Lee, Y.-C., Tzeng, C.-R., Wang, Y.-P., Chang, H.-Y., Lin, Y.-F., & Kao, S.-H. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.01.022 · Cited by 44 · see citing works
Bahall, V., De Barry, L., & Rampersad, A. (2022) · World Journal of Surgical Oncology · doi:10.1186/s12957-022-02553-x · Cited by 22 · see citing works
“The pathogenesis of malignant transformation of endometriosis remains unelucidated; however, certain studies implicate oxidative stress according to a two-step process in endometriotic carcinogenesis [13].”
BackgroundRole of Oxidative Stress and Antioxidant Therapies in Endometriosis
Baboo, K. D., Chen, Z.-Y., & Zhang, X.-M. (2019) · Reproductive and Developmental Medicine · doi:10.4103/2096-2924.268154 · Cited by 20 · see citing works
“Accumulating evidence indicates that oxidative stress (OS) plays an important role in the etiology of EMS.[2,3] It is reported to play an active role in the initiation, maintenance, and progression of the disease.”
BackgroundUnveil the pain of endometriosis: from the perspective of the nervous system
Fan, P., & Li, T. (2022) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2022.26 · Cited by 20 · see citing works
The Impact of Laparoscopic Surgery on Fertility Outcomes in Patients with Minimal/Mild Endometriosis
Grigoriadis, G., Roman, H., Gkrozou, F., & Daniilidis, A. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13164817 · Cited by 10 · see citing works
The Impact of Laparoscopic Surgery on Fertility Outcomes in Patients with Minimal/Mild Endometriosis
Grigoriadis, G., & Daniilidis, A. (2024) · doi:10.20944/preprints202407.0446.v1 · Cited by 10 · see citing works
- Authors
- Scutiero, G., Iannone, P., Bernardi, G., Bonaccorsi, G., Spadaro, S., Volta, C. A., Greco, P., & Nappi, L.
- Affiliations
- University of Ferrara (IT)
- University of Foggia (IT)
- Corresponding author
- Iannone, Piergiorgio
- ORCID
- Venue
- Oxidative Medicine and Cellular Longevity
- Publisher
- Wiley
- Published
- 2017-01
- Volume
- 2017
- Issue
- 1
- Pages
- 7265238-7265238
- ISSN
- 1942-0994 (ISSN-L)
- 1942-0900
- PMC
- PMC5625949
- OpenAlex
- W2754055756
- Cited by
- 436
- References
- 62
- Citations by year
- 2026: 67 · 2025: 74 · 2024: 65 · 2023: 59 · 2022: 46 · 2021: 40 · 2020: 38 · 2019: 34 · 2018: 12 · 2015: 1
- FWCI
- 3.75
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Oxidative Medicine and Cellular Longevity (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Institutional Research Information System University of Ferrara (University of Ferrara) (submittedVersion, cc-by)
- Institutional Research Information System University of Ferrara (University of Ferrara) (submittedVersion)
- Funders
- Università degli Studi di Ferrara
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Biochemistry › Antioxidant Activity and Oxidative Stress
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Keywords
- endometriosis, oxidative stress, reactive oxygen species, antioxidants, iron metabolism, oxidative stress biomarkers, endometriosis-associated infertility, endometriosis-associated cancer, endometriosis pathophysiology, peritonitis, endometriosis etiology
- MeSH terms
- Endometriosis, Female, Humans, Oxidative Stress
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