Oxidative stress biomarkers in patients with endometriosis: systematic review
Abstract
Purpose Since the first description about oxygen toxicity made by Joseph Priestley, the oxidative stress has been enrolled as a key factor in the pathogenesis of endometriosis. Our aim was to review oxidative stress biomarkers measured in patients with endometriosis.Methods Relevant studies were identified by searches of the MEDLINE database from 1990 to March 2011 using endometriosis, free radical and oxidative stress as mesh terms. We only included manuscripts in English, and review articles were excluded. In addition, free radical chemistry and oxidative stress history were discussed.Results After inclusion and exclusion criteria, 19 articles were selected to be included in this systematic review. A total of 36 oxidative stress biomarkers (20 different markers) were measured in patients with endometriosis. Some of the markers were measured in more than one manuscript. They were arranged in five subgroups: Enzymatic activity (n = 3), Anions/free radicals (n = 5), Lipoperoxidation markers (n = 7), DNA Damage markers (n = 1), and Protein oxidation (n = 4). Of those 36 markers, 23 were found to be significantly higher in patients with endometriosis comparing with control patients.Conclusion Oxidative stress plays an important role in the pathogenesis and progression of endometriosis.
Integrity signals
Registry
Cites
Statistics
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?
Of the 36 oxidative stress biomarkers, 23 were significantly higher in patients with endometriosis compared to controls.
“Of those 36 oxidative stress biomarkers, 23 were found to be significantly higher in patients with endometriosis compared to controls.77”
From Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France (2013) · cites this paper as [77]
In a systematic review of oxidative stress biomarkers in patients with endometriosis, 36 biomarkers were identified.
“In a systematic review of oxidative stress biomarkers measured in patients with endometriosis, a total of 36 were identified.”
From Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France (2013) · cites this paper as [77]
Oxidative stress is implicated as a key factor in the pathogenesis of endometriosis.
“Oxidative stress is implicated as a key factor in the pathogenesis of endometriosis.”
From Defining Future Directions for Endometriosis Research: Workshop Report From the 2011 World Congress of Endometriosis in Montpellier, France (2013) · cites this paper as [77]
Cites
Reactive oxygen species: Metabolism, oxidative stress, and signal transduction
Apel, K., & Hirt, H. (2004) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.55.031903.141701 · Cited by 11,723 · see citing works
Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase
Li, Y., Huang, T.-T., Carlson, E. J., Melov, S., Ursell, P. C., Olson, J. L., Noble, L. J., Yoshimura, M. P., Berger, C., Chan, P. H., et al. (1995) · Nature Genetics · doi:10.1038/ng1295-376 · Cited by 1,789 · see citing works
The Haber–Weiss reaction and mechanisms of toxicity
Kehrer, J. P. (2000) · Toxicology · doi:10.1016/s0300-483x(00)00231-6 · Cited by 1,418 · see citing works
Oxygen poisoning and x-irradiation: a mechanism in common
Gerschman, R., Gilbert, D. L., Nye, S. W., Dwyer, P., & Fenn, W. O. (1954) · Science · doi:10.1126/science.119.3097.623 · Cited by 961 · cited 1× · see citing works
“The study demonstrated that antioxidants decrease the damage from x-ray irradiation [7].”
BackgroundSpitz, D. R., Azzam, E. I., Jian Li, J., & Gius, D. (2004) · Cancer and Metastasis Reviews · doi:10.1023/b:canc.0000031769.14728.bc · Cited by 710 · see citing works
Kao, L. C., Germeyer, A., Tulac, S., Lobo, S., Yang, J. P., Taylor, R. N., Osteen, K., Lessey, B. A., & Giudice, L. C. (2003) · Endocrinology · doi:10.1210/en.2003-0043 · Cited by 696 · see citing works
The Haber-Weiss cycle – 70 years later
Koppenol, W. H. (2001) · Redox Report · doi:10.1179/135100001101536373 · Cited by 502 · 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
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
Bert, P., & Brocklehurst, R. J. (1878) · Cited by 307 · 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 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
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
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
Liochev, S. I. (2018) · Routledge eBooks · doi:10.1201/9780203747605-1 · Cited by 129 · 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
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
Observations on different kinds of air
Priestley, J., Hey, W., Basire, J., et al. (1772) · doi:10.5962/bhl.title.62546 · Cited by 123 · see citing works
Wang, Y., Sharma, R. K., Falcone, T., Goldberg, J. M., & Agarwal, A. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00343-9 · Cited by 118 · see citing works
Self-citationThe 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 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
Autoantibodies to markers of oxidative stress are elevated in women with endometriosis
Shanti, A., Santanam, N., Morales, A. J., Parthasarathy, S., & Murphy, A. A. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(99)00145-4 · Cited by 104 · 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
Effects of oxidants and antioxidants on proliferation of endometrial stromal cells
Foyouzi, N., Berkkanoğlu, M., Arici, A. M., Kwintkiewicz, J., Izquierdo, D. M., & Dulęba, A. J. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.02.133 · Cited by 101 · see citing works
BINGER, C. A. L., Faulkner, J. M., & Moore, R. L. (1927) · The Journal of Experimental Medicine · doi:10.1084/jem.45.5.849 · Cited by 81 · see citing works
Ho, H., Wu, M., Chen, S., Chao, K., Chen, C., & Yang, Y. (1997) · Human Reproduction · doi:10.1093/humrep/12.12.2810 · Cited by 73 · see citing works
Xanthine oxidase in eutopic and ectopic endometrium in endometriosis and adenomyosis
Ota, H., Igarashi, S., & Tanaka, T. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01670-3 · Cited by 70 · 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
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
La pression barométrique: Paul Bert's hypoxia theory and its critics
Kellogg, R. H. (1978) · Respiration Physiology · doi:10.1016/0034-5687(78)90046-4 · Cited by 42 · see citing works
The evolution of Free Radical Biology & Medicine: A 20-year history
Davies, K. J. A., & PRYOR, W. A. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.09.001 · Cited by 28 · see citing works
Comparative study of oxidative stress in maternal blood with that of cord blood and maternal milk
Erdem, M., Harma, M., Harma, I. M., et al. (2011) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-011-1993-8 · Cited by 24 · see citing works
Vroman, L. (1977) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1977.tb41799.x · Cited by 23 · see citing works
Slater, M. D., Quagliotto, G., Cooper, M., et al. (2005) · The Histochemical Journal · doi:10.1007/s10735-005-3802-9 · Cited by 18 · see citing works
Özkan, Y., Yardım-Akaydin, S., Erdem, A., et al. (2011) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-011-2150-0 · Cited by 16 · see citing works
Free Radicals Can Kill You: Lavoisier's Oxygen Revolution
Weissmann, G. (2010) · The FASEB Journal · doi:10.1096/fj.10-0301ufm · Cited by 8 · see citing works
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 · 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
Rogers, P. A. W., D’Hooghe, T. M., Fazleabas, A., Giudice, L. C., Montgomery, G. W., Petraglia, F., & Taylor, R. N. (2013) · Reproductive Sciences · doi:10.1177/1933719113477495 · Cited by 154 · 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
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
Arterial stiffness is increased in young women with endometriosis
Tani, A., Yamamoto, S., Maegawa, M., Kunimi, K., Matsui, S., Keyama, K., Kato, T., Uemura, H., Kuwahara, A., Matsuzaki, T., et al. (2015) · Journal of Obstetrics and Gynaecology · doi:10.3109/01443615.2014.992871 · Cited by 37 · see citing works
Could statins constitute a novel treatment for endometriosis? Systematic review of the literature
Gibran, L., Maranhão, R. C., Abrão, M. S., Baracat, E. C., & Podgaec, S. (2014) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.05.028 · Cited by 29 · see citing works
Self-citation
- Authors
- Carvalho, L. F. P., Samadder, A. N., Agarwal, A., Fernandes, L. F. C., & Abrão, M. S.
- Affiliations
- Cleveland Clinic (US)
- Universidade de São Paulo (BR)
- Corresponding author
- Carvalho, Luiz Fernando Pina
- Venue
- Archives of Gynecology and Obstetrics
- Published
- 2012-07-12
- Volume
- 286
- Issue
- 4
- Pages
- 1033-1040
- ISSN
- 0003-9128 (ISSN-L)
- 0932-0067
- 1432-0711
- OpenAlex
- W2063806095
- Cited by
- 140
- References
- 37
- Citations by year
- 2026: 6 · 2025: 15 · 2024: 8 · 2023: 9 · 2022: 11 · 2021: 9 · 2020: 7 · 2019: 8 · 2018: 14 · 2017: 11 · 2016: 10 · 2015: 12 · 2014: 12 · 2013: 7 · 2012: 1
- FWCI
- 1.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Archives of Gynecology and Obstetrics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Biochemistry › Antioxidant Activity and Oxidative Stress
- Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
- Keywords
- endometriosis, oxidative stress, oxidative stress biomarkers, free radicals, lipid peroxidation, DNA damage, protein oxidation, antioxidant enzymes, endometriosis pathogenesis
- MeSH terms
- Endometriosis, Female, Humans, Biomarkers, 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