Evaluation of Serum and Urinary Angiogenic Factors in Patients with Endometriosis
Open accessAbstract
Problem The aim of this study was to evaluate serum and urinary levels of vascular endothelial growth factors, tumor necrosis factor‐α (TNF‐α), and soluble fms‐like tyrosine kinase (sFlt‐1) in patients with endometriosis. Method of study During surgery for pelvic pain, pelvic mass or infertility, serum and urine were collected. Of 70 patients, 46 had histology‐proven endometriosis and 24 patients without endometriosis participated as controls. Results Serum TNF‐α levels and urinary sFlt‐1 levels corrected for creatinine excretion were significantly increased in the endometriosis group (P = 0.001 and P = 0.011 respectively). Serum sFlt‐1 levels and urinary sFlt‐1 levels corrected for creatinine were significantly higher in patients with minimal‐to‐mild disease (P = 0.014 and P = 0.015 respectively), where serum TNF‐α levels were increased in moderate‐to‐severe endometriosis (P < 0.001). Conclusion The pathogenesis of minimal‐to‐mild endometriosis and moderate‐to‐severe endometriosis seems to be different. Increased sFlt‐1 levels in serum and urine of minimal‐to‐mild disease indicate that sFlt‐1 may have an important role in inhibiting angiogenic process of the disease.
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?
Creatinine-corrected soluble fms-like tyrosine kinase (sFlt-1) is significantly elevated in the urine of women with endometriosis when measured by ELISA.
“Creatinine-corrected soluble fms-like tyrosine kinase (sFlt-1) was found to be significantly elevated in the urine of women with endometriosis using enzyme-linked immunosorbent assays (ELISA) [101].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [101]
Cites
Revised American Society for Reproductive Medicine classification of endometriosis: 1996
American Society for Reproductive Medicine (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81391-x · Cited by 3,018 · see citing works
Dvorak, H. F. (2002) · Journal of Clinical Oncology · doi:10.1200/jco.2002.10.088 · Cited by 1,574 · see citing works
Kendall, R. L., Wang, G., & Thomas, K. A. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1355 · Cited by 730 · see citing works
Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial
Bedaiwy, M. A. (2002) · Human Reproduction · doi:10.1093/humrep/17.2.426 · Cited by 485 · see citing works
Clark, D. E., Smith, S. K., He, Y., Day, K. A., Licence, D. R., Corps, A. N., Lammoglia, R., & Jones, D. S. (1998) · Biology of Reproduction · doi:10.1095/biolreprod59.6.1540 · Cited by 413 · see citing works
Angiogenic Factors in Endometriosis
Taylor, R. N., Lebovic, D. I., & Mueller, M. D. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb02769.x · Cited by 304 · see citing works
Vascular endothelial growth factor and endometriotic angiogenesis
McLaren, J. (2000) · Human Reproduction Update · doi:10.1093/humupd/6.1.45 · Cited by 269 · see citing works
Antiangiogenic Agents Are Effective Inhibitors of Endometriosis
Hull, M. L., Jones, D. S., Chan, C. L. K., Bruner‐Tran, K. L., Osteen, K. G., Tom, B. D. M., Fan, T. D., & Smith, S. K. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021912 · Cited by 243 · see citing works
Iwabe, T., Harada, T., Tsudo, T., Nagano, Y., Yoshida, S., Tanikawa, M., & Terakawa, N. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.2.6335 · Cited by 201 · see citing works
Buhimschi, C. S., Norwitz, E. R., Funai, E. F., Richman, S. M., Guller, S. M., Lockwood, C. J., & Buhimschi, I. A. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.12.052 · Cited by 153 · see citing works
Daraï, É. (2003) · Human Reproduction · doi:10.1093/humrep/deg321 · Cited by 147 · see citing works
Xavier, P., Belo, L., Beires, J., Rebelo, I., Martinez-de-Oliveira, J., Lunet, N., & Barros, H. (2006) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-005-0080-4 · Cited by 130 · see citing works
Krüssel, J.-S. (1999) · Molecular Human Reproduction · doi:10.1093/molehr/5.5.452 · Cited by 101 · see citing works
Levels of vascular endothelial growth factor (VEGF) in serum of patients with endometriosis
Gagné, D. (2003) · Human Reproduction · doi:10.1093/humrep/deg326 · Cited by 68 · see citing works
Vascular endothelial growth factor and interleukin-8 in ovarian cystic pathology
Fasciani, A., D’Ambrogio, G., Bocci, G., Luisi, S. V., Artini, P. G., & Genazzani, A. R. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)01804-0 · Cited by 55 · see citing works
Expression of interleukin-8 receptors in endometriosis
Ulukuş, M., Ulukus, E. C., Seval, Y., Zheng, W., & Arici, A. M. (2004) · Human Reproduction · doi:10.1093/humrep/deh675 · Cited by 52 · see citing works
Yamaguchi, T., Bando, H., Mori, T., Takahashi, K., Matsumoto, H., Yasutome, M., Weich, H. A., & Toi, M. (2007) · Cancer Science · doi:10.1111/j.1349-7006.2007.00402.x · Cited by 52 · see citing works
Soluble VEGF/sFLt1 ratio is an independent predictor of AML patient out come
Aref, S., Sherbiny, M. E., Goda, T., et al. (2005) · Hematology · doi:10.1080/10245330500065797 · Cited by 51 · see citing works
Steff, A., Gagné, D., Pagé, M., Rioux, A., Hugo, P., & Gosselin, D. R. (2004) · American Journal of Reproductive Immunology · doi:10.1046/j.8755-8920.2003.00138.x · Cited by 47 · see citing works
Matsumoto, K., & Kanmatsuse, K. (2001) · PubMed · Cited by 39 · see citing works
İlhan, N., İlhan, N., Ilhan, N., et al. (2004) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2004.03.012 · Cited by 33 · see citing works
Robertson, D. M., Selleck, K., Suikkari, A., et al. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136327 · Cited by 32 · see citing works
McIlhenny, C., George, W. D., & Doughty, J. (2002) · British Journal of Cancer · doi:10.1038/sj.bjc.6600322 · Cited by 32 · see citing works
Soluble FLT-1 is detectable in the sera of colorectal and breast cancer patients.
Kumar, H., Heer, K., Greenman, J., et al. (2002) · PubMed · Cited by 30 · see citing works
Urine vascular endothelial growth factor-A is not a useful marker for endometriosis
Potlog‐Nahari, C., Stratton, P., Winkel, C. A., Widra, E. A., Sinaii, N., Connors, S. L., & Nieman, L. K. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.10.040 · Cited by 24 · see citing works
Different response of urinary excretion of VEGF in patients with chronic and acute renal failure
Kitamoto, Y., Matsuo, K., & Tomita, K. (2001) · Kidney International · doi:10.1046/j.1523-1755.2001.00504.x · Cited by 22 · see citing works
Rivera, M., Taléns‐Visconti, R., Sirera, R., Bertoméu, V., Salvador, A., Cortés, R., de Burgos, F. G., Climent, V. E., Payá, R., Martínez‐Dolz, L., et al. (2004) · European Journal of Heart Failure · doi:10.1016/j.ejheart.2004.03.017 · Cited by 15 · see citing works
Vascular endothelial growth factor and its soluble receptor in ovarian pathology
Artini, P. G., Cristello, F., Monti, M., et al. (2005) · Gynecological Endocrinology · doi:10.1080/09513590500099560 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Peripheral biomarkers of endometriosis: a systematic review
May, K. E., Conduit-Hulbert, S. A., Villar, J., Kirtley, S., Kennedy, S. H., & Becker, C. M. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmq009 · Cited by 418 · see citing works
Endometriosis, assisted reproduction technology, and risk of adverse pregnancy outcome
Stephansson, O., Kieler, H., Granath, F., & Falconer, H. (2009) · Human Reproduction · doi:10.1093/humrep/dep186 · Cited by 234 · see citing works
Update 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 · see citing works
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 · see citing works
Urinary vitamin D-binding protein is elevated in patients with endometriosis
Cho, S., Choi, Y. S., Yim, S. Y., Yang, H. I., Jeon, Y. E., Lee, K. E., Kim, H., Seo, S. K., & Lee, B. S. (2012) · Human Reproduction · doi:10.1093/humrep/der345 · Cited by 74 · see citing works
Self-citationSigns of reduced angiogenic activity after surgical removal of deeply infiltrating endometriosis
Bourlev, V., Iljasova, N., Adamyan, L., Larsson, A., & Olovsson, M. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.02.019 · Cited by 57 · see citing works
Selected cytokines and glycodelin A levels in serum and peritoneal fluid in girls with endometriosis
Drosdzol‐Cop, A., & Skrzypulec‐Plinta, V. (2012) · Journal of Obstetrics and Gynaecology Research · doi:10.1111/j.1447-0756.2012.01860.x · Cited by 52 · see citing works
Reduced Levels of Serum Pigment Epithelium-Derived Factor in Women With Endometriosis
Chen, L., Fan, R., Huang, X., Xu, H., & Zhang, X. (2012) · Reproductive Sciences · doi:10.1177/1933719111413300 · Cited by 26 · see citing works
Brain-Derived Neurotrophic Factor in Plasma of Women with Endometriosis
Giannini, A., Bucci, F., Luisi, S., Cela, V., Pluchino, N., Merlini, S., Casarosa, E., Russo, M., Cubeddu, A., Daino, D., et al. (2010) · Journal of Endometriosis · doi:10.1177/228402651000200305 · Cited by 27 · see citing works
Copeptin is associated with the severity of endometriosis
Tuten, A., Kucur, M., Imamoglu, M., Kaya, B., Acikgoz, A. S., Yilmaz, N., Ozturk, Z., & Oncul, M. (2014) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-014-3163-2 · Cited by 23 · see citing works
- Authors
- Cho, S. H., Oh, Y. J., Nam, A., Kim, H. Y., Park, J. H., Kim, J. H., Park, K. H., Cho, D. J., & Lee, B. S.
- Affiliations
- Yonsei University (KR)
- Corresponding author
- Lee, Byung Seok
- Venue
- American Journal of Reproductive Immunology
- Publisher
- Wiley
- Published
- 2007-11-09
- Volume
- 58
- Issue
- 6
- Pages
- 497-504
- ISSN
- 0271-7352 (ISSN-L)
- 1046-7408
- 1600-0897
- OpenAlex
- W2107597801
- Cited by
- 68
- References
- 28
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 7 · 2023: 3 · 2022: 6 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 2 · 2017: 2 · 2016: 5 · 2015: 6 · 2014: 4 · 2013: 5 · 2012: 5
- FWCI
- 2.95
- Type
- journal article
- Language
- en
- Open access
- Licence
- Locations
- American Journal of Reproductive Immunology (publishedVersion)
- PubMed (publishedVersion)
- YUHSpace (Yonsei University Medical Library) (submittedVersion, cc-by-nc-nd)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
- Keywords
- endometriosis, angiogenic factors, vascular endothelial growth factor, TNF-α, soluble fms-like tyrosine kinase-1, urinary biomarkers, serum biomarkers, endometriosis severity, angiogenesis inhibition, pelvic pain, infertility, pelvic mass
- MeSH terms
- Adult, Endometriosis, Female, Humans, Middle Aged, Tumor Necrosis Factor-alpha, Vascular Endothelial Growth Factor Receptor-1, Vascular Endothelial Growth Factor A, Angiogenesis Inducing Agents
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
