The DOI matches its Crossref record; 224 of the 226 references it cites were found in a registry or an index.
Peripheral biomarkers of endometriosis: a systematic review
Open accessAbstract
BACKGROUND: Endometriosis is estimated to affect 1 in 10 women during the reproductive years. There is often delay in making the diagnosis, mainly due to the non-specific nature of the associated symptoms and the need to verify the disease surgically. A biomarker that is simple to measure could help clinicians to diagnose (or at least exclude) endometriosis; it might also allow the effects of treatment to be monitored. If effective, such a marker or panel of markers could prevent unnecessary diagnostic procedures and/or recognize treatment failure at an early stage. METHODS: We used QUADAS (Quality Assessment of Diagnostic Accuracy Studies) criteria to perform a systematic review of the literature over the last 25 years to assess critically the clinical value of all proposed biomarkers for endometriosis in serum, plasma and urine. RESULTS: We identified over 100 putative biomarkers in publications that met the selection criteria. We were unable to identify a single biomarker or panel of biomarkers that have unequivocally been shown to be clinically useful. CONCLUSIONS: Peripheral biomarkers show promise as diagnostic aids, but further research is necessary before they can be recommended in routine clinical care. Panels of markers may allow increased sensitivity and specificity of any diagnostic test.
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
“Firstly, according to QUADAS (Quality Assessment of Diagnostic Accuracy Studies) guidelines [15,16], samples should be collected at a consistent phase of the cycle and results should be corrected for the cycle phases.”
From A high sensitivity assay is more accurate than a classical assay for the measurement of plasma CRP levels in endometriosis (2011) · cites this paper as [15]
In the citing paper
“Secondly, according to a recently published systematic review, lack of correction for the phase of the menstrual cycle can explain the considerable variability between studies with respect to blood levels of biomarkers in women with endometriosis and controls [15].”
From A high sensitivity assay is more accurate than a classical assay for the measurement of plasma CRP levels in endometriosis (2011) · cites this paper as [15]
In the citing paper
“Studies performed in various compartments in the body as serum, peritoneal, and follicular fluids are not sufficient for precise evaluation [17].”
From Serum levels of androgens and prostate-specific antigen in endometriosis (2014) · cites this paper as [17]
In the citing paper
“In our study, samples were collected at a well defined phase of the cycle and results were corrected for cycle phase, as recommended by the QUADAS (Quality Assessment of Diagnostic Accuracy Studies) guidelines [15,16].”
From A high sensitivity assay is more accurate than a classical assay for the measurement of plasma CRP levels in endometriosis (2011) · cites this paper as [15]
In the citing paper
“Despite the fact that research on biomarkers of endometriosis are still ongoing, there are still no satisfactory results, which makes it impossible to carry out effective laboratory diagnostics used in the diagnosis and monitoring of the treatment of the disease [157].”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [157]
In the citing paper
“The studies showed that a panel of cytokines, rather than a single biomarker, improve sensitivity and specificity values, with some panels showing the ability to discriminate between different stages of disease.”
From Biomarkers in endometriosis: Challenges and opportunities (2017) · cites this paper as [69]
In the citing paper
“Another ovarian tumor marker, CA-19-9, has been shown to be elevated in endometriosis and has a comparable or lower sensitivity than CA-125 for the detection of endometriosis [23].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Despite extensive research, no single biomarker nor a panel of biomarkers in peripheral blood has been validated as a diagnostic test for endometriosis [17, 20].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [20]
In the citing paper
“Overall, most endometriosis biomarker studies have remained at the level of Phase I [23] and only a few have made it to Phase II studies.”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“At present, such a test does not exist [17, 20].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [20]
In the citing paper
“Putative endometriosis biomarkers are mostly glycoproteins, growth or adhesion factors, hormones, or proteins related to immunology or angiogenesis [17, 23, 30].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Levels of the sICAM-I have been suggested to rise during early stages of endometriosis (I-II) and decrease at stage III-IV [23].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Its usefulness as biomarker for endometriosis is unclear, as some studies show elevated blood levels in endometriosis patients while other studies do not record a significant difference [23, 67].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Follistatin, an inhibitor of activin, has been shown to be increased in endometriosis patients [23], especially in a subgroup of patients with ovarian endometrioma, and showed good sensitivity and specificity [43].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“The inflammatory marker C-reactive protein (CRP) has been shown to be upregulated [23], especially when examined with a high sensitivity assay making it possible to detect subclinical inflammation in women with endometriosis [50].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“However, other studies could not find an upregulation [23, 51].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Other growth factors, such as soluble epidermal growth factor (EGF) and platelet-derived growth factor (PDGF) have been investigated, but no difference was found between endometriosis patients and control women [23].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Both total immunoglobulin levels and antiendometrial antibodies have been investigated as potential biomarkers for endometriosis of which the latter showed the most promising results, being more commonly present in endometriosis patients than in controls [23].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Hepatocyte growth factor (HGF) was suggested to be elevated in women with endometriosis [72], although this was not confirmed in an additional study [23, 73].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“These studies have shown promising results; however, proteomics technologies are costly and time-consuming [23], and there is a need for better standardization and reproducibility of proteomic technologies before they can be used reliably in clinical research projects [17].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Elevations of fibroblast growth factor-2 (FGF-2), angiogenin, and soluble Flt-I (VEGFR-1) in serum of women with endometriosis have all been recorded [23].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“A range of cell populations, including T cells, B cells, natural killer (NK) cells, macrophages/monocytes, and polymorphonuclear neutrophils, has been compared between endometriosis patients and healthy controls [23]. However, for none of these populations the utility as an endometriosis biomarker has been proven [23, 96].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“No consensus exists on changes in steroid hormone levels [23].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Contrasting evidence exists on prolactin, leptin, luteinizing hormone (LH), and adiponectin levels in endometriosis patients versus controls, showing either no difference, an increase (prolactin, leptin LH) or a decrease (adiponectin) [23, 75, 76].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
In the citing paper
“Likewise, specific antibodies against carbonic anhydrase, transferrin, α2-HS glycoprotein, lipid peroxide modified rabbit serum albumin, copper oxidized low-density lipoprotein and malondialdehyde-modified low-density lipoprotein, laminin-I, and cardiolipin have shown promise as potential endometriosis biomarkers [23].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [23]
Citations
Cites
Dermyshi, E., Wang, Y., Yan, C., Hong, W., Qiu, G., Gong, X., & Zhang, T. (2017) · Neonatology · doi:10.1159/000454668 · Cited by 24,586
Meta-analysis of Observational Studies in Epidemiology<SUBTITLE>A Proposal for Reporting</SUBTITLE>
Stroup, D. F. (2000) · JAMA · doi:10.1001/jama.283.15.2008 · Cited by 20,623
Biomarkers and surrogate endpoints: Preferred definitions and conceptual framework
Biomarkers Definitions Working Group (2001) · Clinical Pharmacology & Therapeutics · doi:10.1067/mcp.2001.113989 · Cited by 6,771
Park, J., Adoro, S., Guinter, T. I., Erman, B., Alag, A., Catálfamo, M., Kimura, M. Y., Cui, Y., Lucas, P. J., Gress, R. E., et al. (2010) · Nature Immunology · doi:10.1038/ni.1840 · Cited by 5,835
Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M., & Toda, M. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.155.3.1151 · Cited by 5,608
Nagata, S., & Golstein, P. (1995) · Science · doi:10.1126/science.7533326 · Cited by 3,979
Whiting, P., Rutjes, A. W., Reitsma, J. B., Bossuyt, P. M., & Kleijnen, J. (2003) · BMC Medical Research Methodology · doi:10.1186/1471-2288-3-25 · Cited by 3,592
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166
Users' Guides to the Medical Literature
Guyatt, G. H. (1993) · JAMA · doi:10.1001/jama.270.17.2096 · Cited by 3,083
THE JOURNAL OF REPRODUCTIVE MEDICINE
Reddy, D. M., & Wasserman, S. A. (1999) · AJN American Journal of Nursing · doi:10.1097/00000446-199901000-00024 · Cited by 2,483
Research works printed but not linked: 33
- Adamyan, 1993, International journal of fertility, 38, 92
- Arumugam, 1991, The Malaysian journal of pathology, 13, 43
- BADAWY, 1984, Obstetrics & Gynecology, 63, 271
- Badawy, 1987, The Journal of reproductive medicine, 32, 194
- Barrier, 2002, Journal of the Society for Gynecologic Investigation, 9, 98, 10.1016/S1071-5576(01)00158-7 · DOI
- Borkowski, 2008, Post py higieny i medycyny do ?wiadczalnej (Online), 62, 103
- Fu, 2002, Chinese medical sciences journal = Chung-kuo i hs eh k'o hs eh tsa chih / Chinese Academy of Medical Sciences, 17, 121
- Garza, 1991, The Journal of reproductive medicine, 36, 177
- 1993, Obstetrics & Gynecology, 81, 665
- 2007, ARCH MED SCI, 3, 37
- Hadfield, 1996, Human Reproduction, 11, 878, 10.1093/humrep/ · DOI
- Ho, 1995, Human Reproduction, 10, 2671, 10.1093/humrep/ · DOI
- Iwasaki, 1993, International journal of fertility and menopausal studies, 38, 229
- 2008, Fertility and sterility, 92, 1221
- Linghu, 2004, Chinese medical sciences journal = Chung-kuo i hs eh k'o hs eh tsa chih / Chinese Academy of Medical Sciences, 19, 56
- 1997, AUST J MED SCI, 18, 56
- 1997, AUST J MED SCI, 18, 116
- Matalliotakis, 1997, International journal of fertility and women's medicine, 42, 211
- Matalliotakis, 2000, American journal of obstetrics and gynecology, 183, 58, 10.1016/S0002-9378(00)78147-6 · DOI
- Matalliotakis, 2003, Journal of the Society for Gynecologic Investigation, 10, 118, 10.1016/S1071-55760200261-7 · DOI
- Matalliotakis, 2004, International journal of fertility and women's medicine, 49, 75
- Molo, 1994, The Journal of reproductive medicine, 39, 964
- 1991, Obstetrics & Gynecology, 165, 1857
- Odukoya, 1995, Human Reproduction, 10, 942, 10.1093/humrep/ · DOI
- Odukoya, 1995, Human Reproduction, 10, 1214, 10.1093/humrep/ · DOI
- Radwanska, 1987, The Journal of reproductive medicine, 32, 605
- Rajkumar, 1992, The Journal of reproductive medicine, 37, 552
- Tanaseanu, 2007, European journal of medical research, 12, 145
- VERCELLINI, 1992, Obstetrics & Gynecology, 79, 743
- Vigano, 2002, Journal of Clinical Endocrinology & Metabolism, 87, 1085, 10.1210/jc.87.3.1085 · DOI
- WILD, 1991, Obstetrics & Gynecology, 77, 927
- Zhang, 2005, Acta obstetricia et gynecologica Scandinavica, 84, 297, 10.1080/j.0001-6349.2005.00679.x · DOI
- Zong, 2003, Di yi jun yi da xue xue bao = Academic journal of the First Medical College of PLA, 23, 757
Cited by
Sorted by citations
ESHRE guideline: management of women with endometriosis
Dunselman, G. A. J., Vermeulen, N., Becker, C., Calhaz-Jorge, C., D'Hooghe, T., De Bie, B., Heikinheimo, O., Horne, A. W., Kiesel, L., Nap, A., et al. (2014) · Human Reproduction · doi:10.1093/humrep/det457 · Cited by 2,211
Self-citationESHRE guideline: endometriosis
Becker, C. M., Bokor, A., Heikinheimo, O., Horne, A., Jansen, F., Kiesel, L., King, K., Kvaskoff, M., Nap, A., Petersen, K., et al. (2022) · Human Reproduction Open · doi:10.1093/hropen/hoac009 · Cited by 1,712
“…should not use measurement of biomarkers in endometrial tissue, blood, menstrual or uterine fluids to diagnose endometriosis (Mol et al. , 1998; May et al. , 2010; May et al. , 2011; Liu et al. , 2015; Cosar et al. , 2016; Gupta et al. , 2016; Hirsch et al. , 2016; Nisenblat et al. , 2016a;…”
Self-citationEndometriosis is a chronic systemic disease: Clinical challenges and novel innovations
Taylor, H. S., Kotlyar, A. M., & Flores, V. A. (2021) · The Lancet · doi:10.1016/s0140-6736(21)00389-5 · Cited by 1,425
Zondervan, K. T., Becker, C. M., Koga, K., Missmer, S. A., Taylor, R. N., & Viganò, P. (2018) · Nature Reviews Disease Primers · doi:10.1038/s41572-018-0008-5 · Cited by 1,257
Self-citationSmolarz, B., Szyłło, K., & Romanowicz, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910554 · Cited by 560
Consensus on current management of endometriosis
Johnson, N. P., Hummelshoj, L., for the World Endometriosis Society Montpellier Consortium, Abrao, M. S., Adamson, G. D., Allaire, C., Amelung, V., Andersson, E., Becker, C., Birna Árdal, K. B., et al. (2013) · Human Reproduction · doi:10.1093/humrep/det050 · Cited by 558
Self-citationThe association between endometriosis and autoimmune diseases: a systematic review and meta-analysis
Shigesi, N., Kvaskoff, M., Kirtley, S., Feng, Q., Fang, H., Knight, J. C., Missmer, S. A., Rahmioglu, N., Zondervan, K. T., & Becker, C. M. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz014 · Cited by 382
Self-citationBlood biomarkers for the non-invasive diagnosis of endometriosis
Nisenblat, V., Bossuyt, P. M., Shaikh, R., Farquhar, C. M., Jordan, V., Scheffers, C. S., Mol, B. W., JOHNSON, N. P., & Hull, M. L. (2016) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012179 · Cited by 401
Incidence of endometriosis by study population and diagnostic method: the ENDO study
Buck Louis, G. M., Hediger, M. L., Peterson, C. M., Croughan, M., Sundaram, R., Stanford, J., Chen, Z., Fujimoto, V. Y., Varner, M. W., Trumble, A., et al. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.05.087 · Cited by 309
Impacts of endocrine disrupting chemicals on reproduction in wildlife and humans
Marlatt, V. L., Bayen, S., Castañeda-Cortés, D. C., Delbès, G., Grigorova, P., Langlois, V. S., Martyniuk, C. J., Metcalfe, C. D., Parent, L., Rwigemera, A., et al. (2021) · Environmental Research · doi:10.1016/j.envres.2021.112584 · Cited by 297
Maddern, J., Grundy, L., Castro, J., & Brierley, S. M. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.590823 · Cited by 298
Biomarkers in endometriosis: Challenges and opportunities
Ahn, S. H., Singh, V., & Tayade, C. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.01.009 · Cited by 242
Endometrial alterations in endometriosis: a systematic review of putative biomarkers
May, K. E., Villar, J., Kirtley, S., Kennedy, S. H., & Becker, C. M. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr013 · Cited by 237
Self-citationCombination of the non-invasive tests for the diagnosis of endometriosis
Nisenblat, V., Prentice, L., Bossuyt, P. M., Farquhar, C. M., Hull, M. L., & JOHNSON, N. P. (2016) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012281 · Cited by 231
Dyson, M. T., Roqueiro, D., Monsivais, D., Ercan, C. M., Pavone, M. E., Brooks, D. C., Kakinuma, T., Ono, M., Jafari, N., Dai, Y., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004158 · Cited by 211
Accurate diagnosis of endometriosis using serum microRNAs
Moustafa, S. M., Burn, M. S., Mamillapalli, R., Nematian, S., Flores, V. A., & Taylor, H. S. (2020) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2020.02.050 · Cited by 218
Becker, C. M., Laufer, M. R., Stratton, P., Hummelshoj, L., Missmer, S. A., Zondervan, K. T., Adamson, G. D., Adamson, G. D., Allaire, C., Anchan, R., et al. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.07.709 · Cited by 206
Self-citationBiomarkers for the Noninvasive Diagnosis of Endometriosis: State of the Art and Future Perspectives
Anastasiu, C. V., Moga, M., Neculau, A. E., Bălan, A., Scârneciu, I., Dragomir, R. M., Dull, A.-M., & Chicea, L.-M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051750 · Cited by 202
Extrapelvic endometriosis: a rare entity or an under diagnosed condition?
Machairiotis, N., Stylianaki, A., Dryllis, G., Zarogoulidis, P., Kouroutou, P., Tsiamis, N., Katsikogiannis, N., Sarika, E., Courcoutsakis, N. A., Tsiouda, T., et al. (2013) · Diagnostic Pathology · doi:10.1186/1746-1596-8-194 · Cited by 203
Serum microRNAs as diagnostic markers of endometriosis: a comprehensive array-based analysis
Çoşar, E., Mamillapalli, R., Ersoy, G. Ş., Cho, S., Seifer, B. J., & Taylor, H. S. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.04.013 · Cited by 201
Peripheral changes in endometriosis-associated pain
Morotti, M., Vincent, K., Brawn, J., Zondervan, K. T., & Becker, C. M. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu021 · Cited by 198
Self-citationUpdate 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
“Follistatin, an inhibitor of activin, has been shown to be increased in endometriosis patients [23], especially in a subgroup of patients with ovarian endometrioma, and showed good sensitivity and specificity [43].”
InfluentialWang, W.-T., Zhao, Y.-N., Han, B.-W., Hong, S.-J., & Chen, Y.-Q. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2415 · Cited by 193
Anti-inflammatory cytokines in endometriosis
Zhou, W., Yang, H., Shao, J., Mei, J., Chang, K., Zhu, R., & Li, M. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03056-x · Cited by 198
Evaluation 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
Diagnosis of endometriosis in the 21st century
Kiesel, L., & Sourouni, M. (2019) · Climacteric · doi:10.1080/13697137.2019.1578743 · Cited by 192
Nanotechnology in reproductive medicine: Emerging applications of nanomaterials
Barkalina, N., Charalambous, C., Jones, C., & Coward, K. (2014) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2014.01.001 · Cited by 192
Peter, A. W., Adamson, G. D., Al‐Jefout, M., Becker, C. M., D’Hooghe, T. M., Dunselman, G. A. J., Fazleabas, A. T., Giudice, L. C., Horne, A. W., Hull, M. L., et al. (2016) · Reproductive Sciences · doi:10.1177/1933719116654991 · Cited by 192
Self-citationEndometriosis induces gut microbiota alterations in mice
Yuan, M., Li, D., Zhang, Z., Sun, H., An, M., & Wang, G. (2017) · Human Reproduction · doi:10.1093/humrep/dex372 · Cited by 183
Circulating microRNAs as potential biomarkers for endometriosis
Cho, S., Mutlu, L., Grechukhina, O., & Taylor, H. S. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.02.013 · Cited by 181
Association Between Endometriosis and Hypercholesterolemia or Hypertension
Mu, F., Rich-Edwards, J., Rimm, E. B., Spiegelman, D., Forman, J. P., & Missmer, S. A. (2017) · Hypertension · doi:10.1161/hypertensionaha.117.09056 · Cited by 180
Plasma miR-17-5p, miR-20a and miR-22 are down-regulated in women with endometriosis
Jia, S.-Z., Yang, Y., Lang, J., Sun, P., & Leng, J. (2013) · Human Reproduction · doi:10.1093/humrep/des413 · Cited by 172
Endometriosis and the microbiome: a systematic review
Leonardi, M., Hicks, C., El‐Assaad, F., El-Omar, E. M., & Condous, G. S. (2019) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.15916 · Cited by 182
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
The management of menopause in women with a history of endometriosis: A systematic review
Gemmell, L. C., Webster, K. E., Kirtley, S., Vincent, K., Zondervan, K. T., & Becker, C. M. (2017) · Human Reproduction Update · doi:10.1093/humupd/dmx011 · Cited by 154
Self-citationDiagnostic accuracy of cancer antigen 125 for endometriosis: A systematic review and meta-analysis
Hirsch, M., Duffy, J., Davis, C., Nieves Plana, M., Khan, K., & on behalf of the International Collaboration to Harmonise Outcomes and Measures for Endometriosis (2016) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.14055 · Cited by 156
Fassbender, 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
Endocrine disrupting chemicals and endometriosis
Smarr, M. M., Kannan, K., & Louis, G. M. B. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.06.034 · Cited by 149
Nnoaham, K. E., Hummelshøj, L., Kennedy, S., Jenkinson, C., & Zondervan, K. T. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.04.022 · Cited by 149
Self-citationDiscovery of phosphatidylcholines and sphingomyelins as biomarkers for ovarian endometriosis
Vouk, K., Hevir, N., Ribič-Pucelj, M., Haarpaintner, G., Scherb, H., Osredkar, J., Möller, G., Prehn, C., Rižner, T. L., & Adamski, J. (2012) · Human Reproduction · doi:10.1093/humrep/des152 · Cited by 143
Vasculogenesis: A new piece of the endometriosis puzzle
Laschke, M. W., Giebels, C., & Menger, M. D. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr023 · Cited by 136
Agrawal, S., Tapmeier, T. T., Rahmioğlu, N., Kirtley, S., Zondervan, K. T., & Becker, C. M. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020599 · Cited by 137
Self-citationBasic mechanisms of vascularization in endometriosis and their clinical implications
Laschke, M. W., & Menger, M. D. (2018) · Human Reproduction Update · doi:10.1093/humupd/dmy001 · Cited by 131
Monsanto, S. P., Edwards, A. K., Zhou, J., Nagarkatti, P. S., Nagarkatti, M., Young, S. L., Lessey, B. A., & Tayade, C. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.11.047 · Cited by 126
Plasma miRNAs as biomarkers for endometriosis
Vanhie, A., Dolores Saavedra, O., Peterse, D., Beckers, A., Cuéllar, A., Fassbender, A., Meuleman, C., Mestdagh, P., & D’Hooghe, T. M. (2019) · Human Reproduction · doi:10.1093/humrep/dez116 · Cited by 126
Dutta, M., Joshi, M., Srivastava, S., Lodh, I., Chakravarty, B., & Chaudhury, K. (2012) · Molecular BioSystems · doi:10.1039/c2mb25353d · Cited by 121
Peritoneal fluid cytokines related to endometriosis in patients evaluated for infertility
Jørgensen, H., Hill, A. S., Beste, M. T., Kumar, M. P., Chiswick, E. L., Fedorcsák, P., Isaacson, K., Lauffenburger, D. A., Griffith, L. G., & Qvigstad, E. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.03.013 · Cited by 120
Rekker, K., Saare, M., Roost, A. M., Kaart, T., Sõritsa, D., Karro, H., Sõritsa, A., Simón, C., Salumets, A., & Peters, M. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.06.029 · Cited by 118
Molecular aspects of development and regulation of endometriosis
Aznaurova, Y. B., M.B.Zhumataev, M. B. Z., Roberts, T. K., Aliper, A. M., & Zhavoronkov, A. A. (2014) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-12-50 · Cited by 116
Gut Microbiota Exceeds Cervical Microbiota for Early Diagnosis of Endometriosis
Huang, L., Liu, B., Liu, Z., Feng, W.-Q., Liu, M., Wang, Y., Peng, D., Fu, X., Zhu, H., Cui, Z., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.788836 · Cited by 118
Burns, K. A., Thomas, S. Y., Hamilton, K. J., Young, S. L., Cook, D. N., & Korach, K. S. (2017) · Endocrinology · doi:10.1210/en.2017-00562 · Cited by 116
Immunological Basis of the Endometriosis: The Complement System as a Potential Therapeutic Target
Agostinis, C., Balduit, A., Mangogna, A., Zito, G., Romano, F., Ricci, G., Kishore, U., & Bulla, R. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.599117 · Cited by 123
Can chemokines be used as biomarkers for endometriosis? A systematic review
Borrelli, G. M., Abrao, M. S., & Mechsner, S. (2014) · Human Reproduction · doi:10.1093/humrep/det401 · Cited by 102
Nanoparticles in pregnancy: the next frontier in reproductive therapeutics
Pritchard, N., Kaitu’u‐Lino, T. J., Harris, L. K., Tong, S., & Hannan, N. J. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa049 · Cited by 101
Serum and peritoneal interleukin-33 levels are elevated in deeply infiltrating endometriosis
Santulli, P., Borghese, B., Chouzenoux, S., Vaiman, D., Borderie, D., Streuli, I., Goffinet, F., de Ziegler, D., Weill, B. J., Batteux, F., et al. (2012) · Human Reproduction · doi:10.1093/humrep/des154 · Cited by 103
The gut microbiota: a puppet master in the pathogenesis of endometriosis?
Laschke, M. W., & Menger, M. D. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.02.036 · Cited by 95
Urinary biomarkers for the non-invasive diagnosis of endometriosis
Liu, E., Nisenblat, V., Farquhar, C. M., Fraser, I. S., Bossuyt, P. M., JOHNSON, N. P., & Hull, M. L. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012019 · Cited by 91
Papari, E., Noruzinia, M., Kashani, L., & Foster, W. G. (2020) · Fertility and Sterility · doi:10.1016/j.fertnstert.2020.01.026 · Cited by 89
Jones, R. L., Tanadini‐Lang, S., Kendziorski, J. A., Greene, A., & Burns, K. A. (2018) · Environmental Health Perspectives · doi:10.1289/ehp3802 · Cited by 88
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
Polymorphisms and endometriosis: A systematic review and meta-analyses
Méar, L., Herr, M., Fauconnier, A., Pineau, C., & Vialard, F. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmz034 · Cited by 85
Vouk, K., Ribič-Pucelj, M., Adamski, J., & Rižner, T. L. (2016) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2016.02.023 · Cited by 84
Characterization of exosomes in peritoneal fluid of endometriosis patients
Nazri, H. M., Imran, M., Fischer, R., Heilig, R., Manek, S., Dragovic, R., Kessler, B. M., Zondervan, K. T., Tapmeier, T. T., & Becker, C. M. (2020) · Fertility and Sterility · doi:10.1016/j.fertnstert.2019.09.032 · Cited by 84
Self-citationReducing low-value care in endometriosis between limited evidence and unresolved issues: a proposal
Vercellini, P., Giudice, L. C., Evers, J. L. H., & Abrao, M. S. (2015) · Human Reproduction · doi:10.1093/humrep/dev157 · Cited by 76
Cordeiro, F. B., Cataldi, T. R., Perkel, K. J., da Costa, L. D. V. T., Rochetti, R. C., Stevanato, J., Eberlin, M. N., Zylbersztejn, D. S., Cedenho, A. P., & Turco, E. G. L. (2015) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-015-0592-1 · Cited by 75
Soluble VCAM-1/soluble ICAM-1 ratio is a promising biomarker for diagnosing endometriosis
Kuessel, L., Wenzl, R. J., Proestling, K., Balendran, S., Pateisky, P., Yotova, Yerlikaya‐Schatten, G., Streubel, B., & Husslein, H. (2017) · Human Reproduction · doi:10.1093/humrep/dex028 · Cited by 76
Metabolomics reveals perturbations in endometrium and serum of minimal and mild endometriosis
Dutta, M., Singh, B. K., Joshi, M. V., Das, D., Subramani, E., Maan, M., Jana, S. K., Sharma, U., Das, S., Dasgupta, S., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-23954-7 · Cited by 75
Metabolic Profile of Patients with Severe Endometriosis: a Prospective Experimental Study
Murgia, F., Angioni, S. L., D’Alterio, M. N., Pirarba, S., Noto, A., Santoru, M. L., Tronci, L., Fanos, V., Atzori, L., & Congiu, F. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00370-9 · Cited by 73
Endometriosis and possible inflammation markers
Wu, M., Hsiao, K., & Tsai, S. (2015) · Gynecology and Minimally Invasive Therapy · doi:10.1016/j.gmit.2015.05.001 · Cited by 78
New biomarkers in endometriosis
(2019) · Advances in clinical chemistry · doi:10.1016/bs.acc.2018.12.002 · Cited by 72
Rediscovering peritoneal macrophages in a murine endometriosis model
Yuan, M., Li, D., An, M., Li, Q., Zhang, L., & Wang, G. (2016) · Human Reproduction · doi:10.1093/humrep/dew274 · Cited by 71
Morelli, M. A. C., Iuliano, A., Schettini, S. C. A., Petruzzi, D., Ferri, A., Colucci, P., Viggiani, L., Cuviello, F., & Ostuni, A. (2019) · Metabolomics · doi:10.1007/s11306-019-1481-x · Cited by 70
Hirsch, M., Duffy, J. M., Deguara, C. S., Davis, C., & Khan, K. S. (2016) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2016.12.002 · Cited by 73
Liu, M.-H., Liu, X., Zhang, Y., & Guo, S. (2012) · Reproductive Sciences · doi:10.1177/1933719111424453 · Cited by 68
P-selectin as a potential therapeutic target for endometriosis
Guo, S., Ding, D., Geng, J.-G., Wang, L., & Liu, X. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.01.001 · Cited by 68
Recurrent endometriosis: a battle against an unknown enemy
Ceccaroni, M., Bounous, V. E., Clarizia, R., Mautone, D., & Mabrouk, M. (2019) · The European Journal of Contraception & Reproductive Health Care · doi:10.1080/13625187.2019.1662391 · Cited by 67
Assessing brain-derived neurotrophic factor as a novel clinical marker of endometriosis
Wessels, J. M., Kay, V. R., Leyland, N. A., Agarwal, S. K., & Foster, W. G. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.09.003 · Cited by 66
Resveratrol and endometriosis: In vitro and animal studies and underlying mechanisms (Review)
Kolahdouz‐Mohammadi, R., & Arablou, T. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.04.078 · Cited by 69
Persistent Lipophilic Environmental Chemicals and Endometriosis: The ENDO Study
Louis, G. M. B., Chen, Z., Peterson, C. M., Hediger, M. L., Croughan, M. S., Sundaram, R., Stanford, J. B., Varner, M. W., Fujimoto, V. Y., Giudice, L. C., et al. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104432 · Cited by 64
Vicente-Muñoz, S., Morcillo, I., Puchades‐Carrasco, L., Payá, V., Pellicer, A., & Pineda‐Lucena, A. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.07.1149 · Cited by 65
Li, J., Guan, L., Zhang, H., Gao, Y., Sun, J., Gong, X., Li, D., Chen, P., Liang, X., Huang, M., et al. (2018) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-018-0360-z · Cited by 65
Surgery accelerates the development of endometriosis in mice
Long, Q., Liu, X., & Guo, S. (2016) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2016.02.055 · Cited by 62
Kasvandik, S., Samuel, K., Peters, M., Eimre, M., Peet, N., Roost, A. M., Padrik, L., Paju, K., Peil, L., & Salumets, A. (2015) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00965 · Cited by 61
Evidence for a Hypercoagulable State in Women With Ovarian Endometriomas
Wu, Q., Ding, D., Liu, X., & Guo, S. (2015) · Reproductive Sciences · doi:10.1177/1933719115572478 · Cited by 60
Serum miR-17, IL-4, and IL-6 levels for diagnosis of endometriosis
Wang, F., Wang, H., Jin, D., & Zhang, Y. (2018) · Medicine · doi:10.1097/md.0000000000010853 · Cited by 62
Endometriosis is associated with aberrant metabolite profiles in plasma
Letsiou, S., Peterse, D. P., Fassbender, A., Hendriks, M. M. W. B., van den Broek, N. J. F., Berger, R., O, D. F., Vanhie, A., Vodolazkaia, A., Langendonckt, A. V., et al. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.12.032 · Cited by 58
Carmona, F., Chapron, C., Martínez‐Zamora, M. Á., Santulli, P., Rabanal, A., Martínez‐Florensa, M., Lozano, F., & Balasch, J. (2012) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2012.06.001 · Cited by 59
Structure, Function, and Evaluation of the Female Reproductive Tract
Lessey, B. A., & Young, S. L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-323-47912-7.00009-3 · Cited by 60
Irritable bowel syndrome and endometriosis: New insights for old diseases
Viganò, D., Zara, F., & Usai, P. (2017) · Digestive and Liver Disease · doi:10.1016/j.dld.2017.12.017 · Cited by 57
Discovery of non-invasive biomarkers for the diagnosis of endometriosis
Irungu, S., Mavrelos, D., Worthington, J., Blyuss, O. B., Sarıdoğan, E., & Timms, J. F. (2019) · Clinical Proteomics · doi:10.1186/s12014-019-9235-3 · Cited by 55
Malignant Transformation and Associated Biomarkers of Ovarian Endometriosis: A Narrative Review
Михалева, Л. М., Davydov, A. I., Игоревна, П. О., Вячеславовна, М. Е., Nikolenko, V. N., Неганова, М. Е., Klochkov, S. G., Somasundaram, S. G., Kirkland, C. E., & Aliev, G. (2020) · Advances in Therapy · doi:10.1007/s12325-020-01363-5 · Cited by 60
Panels of Cytokines and Other Secretory Proteins as Potential Biomarkers of Ovarian Endometriosis
Kocbek, V., Vouk, K., Bersinger, N. A., Mueller, M. D., & Rižner, T. L. (2015) · Journal of Molecular Diagnostics · doi:10.1016/j.jmoldx.2015.01.006 · Cited by 54
Vascular endothelial growth factor pathway in endometriosis: genetic variants and plasma biomarkers
Vodolazkaia, A., Yesilyurt, B. T., Kyama, C. M., Bokor, A., Schols, D., Huskens, D., Meuleman, C., Peeraer, K., Tomassetti, C., Bossuyt, X., et al. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.12.016 · Cited by 54
O, D. F., Flores, I., Waelkens, E., & D’Hooghe, T. M. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.04.001 · Cited by 55
Noninvasive biomarkers of endometriosis: myth or reality?
Lanišnik Rižner, T. (2014) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.2014.899905 · Cited by 52
Guo, J. H., Chen, L., Luo, N., Li, C., Chen, R., Qu, X., Liu, M., Kang, L., & Cheng, Z. (2016) · Scientific Reports · doi:10.1038/srep21416 · Cited by 53
Lee, Y. H., Liang, C., Fang, J., Chern, B. S. M., Tan, H. H., & Chan, J. K. Y. (2016) · Scientific Reports · doi:10.1038/srep26117 · Cited by 52
Proteomics 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
Kimber-Trojnar, Ż., Pilszyk, A., Niebrzydowska-Tatus, M., Pilszyk, Z., Ruszała, M., & Leszczyńska‐Gorzelak, B. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10132762 · Cited by 54
Lipidomic profiling of endometrial fluid in women with ovarian endometriosis†
Domı́nguez, F., Ferrando, M., Díaz-Gimeno, P., Quintana, F., Fernández, G., Castells, I., & Simón, C. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox014 · Cited by 50
Metadata
- Authors
- May, K. E., Conduit-Hulbert, S. A., Villar, J., Kirtley, S., Kennedy, S. H., & Becker, C. M.
- Affiliations
- John Radcliffe Hospital (GB)
- Corresponding author
- Becker, C. M.
- Venue
- Human Reproduction Update
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-05-12
- Volume
- 16
- Issue
- 6
- Pages
- 651-674
- ISSN
- 1355-4786 (ISSN-L)
- 1460-2369
- PMC
- PMC2953938
- OpenAlex
- W2160282642
- Cited by
- 418
- References
- 226
- Citations by year
- 2026: 15 · 2025: 13 · 2024: 13 · 2023: 24 · 2022: 37 · 2021: 29 · 2020: 37 · 2019: 36 · 2018: 27 · 2017: 33 · 2016: 38 · 2015: 32 · 2014: 32 · 2013: 18 · 2012: 23
- FWCI
- 2.34
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Human Reproduction Update (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Explore Bristol Research (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Obstetrics and Gynecology › Ectopic Pregnancy Diagnosis and Management
- Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
- Keywords
- endometriosis, peripheral biomarkers, diagnostic biomarkers, serum biomarkers, plasma biomarkers, urinary biomarkers, biomarker panel, diagnostic accuracy, treatment monitoring, delayed diagnosis
- MeSH terms
- Antibodies, Cell Adhesion, Endometriosis, Female, Glycoproteins, Hormones, Humans, Leukocytes, Biomarkers, Cytokines, Apoptosis, Intercellular Signaling Peptides and Proteins, Proteomics, Vascular Endothelial Growth Factor A
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