Evaluation of elevated urinary enolase I levels in patients with endometriosis
Open accessAbstract
OBJECTIVE: The aim of this study is to validate and investigate the clinical value of urinary enolase I in patients with endometriosis. METHODS: Urine samples of 39 patients with histologically confirmed endometriosis and 20 patients without endometriosis were collected. Western blot analysis and enzyme-linked immunosorbent assay were used to detect the increase of enolase I in patients' urine. RESULTS: Urinary enolase I expression corrected for creatinine ratio (non neuronal enolase (NNE)-Cr) was significantly greater in patients with endometriosis (p = 0.026). When the diagnostic performance of NNE-Cr was evaluated with serum CA-125 combination, the area under the curve was 0.821 (95% confidence interval 0.713-0.928) with sensitivity and specificity of 76.9% and 85.0%, respectively. CONCLUSION: Elevated urinary enolase I, in conjunction with serum CA-125, may be used as a potential biomarker for endometriosis.
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Enolase-1 lacked sufficient diagnostic power as an individual analyte (sensitivity 56% and specificity 72%) in a separate study.
“Despite elevation in women with endometriosis, enolase-1 lacked sufficient diagnostic power as an individual analyte (sensitivity 56% and specificity 72%) in a separate study [108].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [108]
Cites
The meaning and use of the area under a receiver operating characteristic (ROC) curve.
Hanley, J. A., & McNeil, B. J. (1982) · Radiology · doi:10.1148/radiology.143.1.7063747 · Cited by 21,856 · see citing works
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
The Biology of Chemokines and their Receptors
Rossi, D., & Zlotnik, A. (2000) · Annual Review of Immunology · doi:10.1146/annurev.immunol.18.1.217 · Cited by 2,410 · 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
Delay in the diagnosis of endometriosis: a survey of women from the USA and the UK
Hadfield, R., Mardon, H., Barlow, D., & Kennedy, S. (1996) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a019270 · Cited by 517 · see citing works
Decramer, S., de Peredo, A. G., Breuil, B., Mischak, H., Monsarrat, B., Bascands, J., & Schanstra, J. P. (2008) · Molecular & Cellular Proteomics · doi:10.1074/mcp.r800001-mcp200 · Cited by 446 · see citing works
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
The performance of CA-125 measurement in the detection of endometriosis: a meta-analysis
Mol, B. W. J., Bayram, N., Lijmer, J. G., Wiegerinck, M. A. H. M., Bongers, M. Y., van der Veen, F., & Bossuyt, P. M. M. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00355-0 · Cited by 355 · see citing works
Diagnostic delay in women with pain and endometriosis
Husby, G. K., Haugen, R. S., & Moen, M. H. (2003) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1034/j.1600-0412.2003.00168.x · Cited by 298 · see citing works
Application of ’omics technologies to biomarker discovery in inflammatory lung diseases
Wheelock, C. E., Goss, V. M., Balgoma, D., Nicholas, B., Brandsma, J., Skipp, P. J. S., Snowden, S. G., Burg, D. W., D’Amico, A., Horváth, I., et al. (2013) · European Respiratory Journal · doi:10.1183/09031936.00078812 · Cited by 271 · see citing works
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 · see citing works
Cytokine profiles in serum and peritoneal fluid from infertile women with and without endometriosis
Kalu, E., Sumar, N., Giannopoulos, T., Patel, P., Croucher, C., Sherriff, E., & Bansal, A. S. (2007) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2007.00569.x · Cited by 173 · see citing works
Prospects for urinary proteomics: Exosomes as a source of urinary biomarkers (Review Article)
Hoorn, E. J., Pisitkun, T., Zietse, R., Gross, P. A., FROKIAER, J., Wang, N. S., Gonzales, P. A., Star, R. A., & Knepper, M. A. (2005) · Nephrology · doi:10.1111/j.1440-1797.2005.00387.x · Cited by 172 · see citing works
Non-invasive diagnosis of endometriosis based on a combined analysis of six plasma biomarkers
Mihalyi, A., Gevaert, O., Kyama, C. M., Simsa, P., Pochet, N., De Smet, F., De Moor, B., Meuleman, C., Billen, J., Blanckaert, N., et al. (2010) · Human Reproduction · doi:10.1093/humrep/dep425 · Cited by 161 · see citing works
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 · see citing works
Bahk, Y. Y., Kim, S. A., Kim, J., Euh, H. J., Bai, G., Cho, S., & Kim, Y. S. (2004) · PROTEOMICS · doi:10.1002/pmic.200400980 · Cited by 144 · see citing works
Self-citationAutoantibodies specific for alpha-enolase in systemic autoimmune disorders.
Pratesi, F., Moscato, S., Sabbatini, A., CHIMENTI, D., Bombardieri, S., & Migliorini, P. (2000) · PubMed · Cited by 124 · see citing works
Proteomics‐based identification of α‐enolase as a tumor antigen in non‐small lung cancer
He, P., Naka, T., Serada, S., Fujimoto, M., Tanaka, T., Hashimoto, S., Shima, Y., Yamadori, T., Suzuki, H., Hirashima, T., et al. (2007) · Cancer Science · doi:10.1111/j.1349-7006.2007.00509.x · Cited by 114 · see citing works
Catalase and α-enolase: two novel granulocyte autoantigens in inflammatory bowel disease (IBD)
Roozendaal, C., Zhao, M., Horst, G., Lockwood, C. M., Kleibeuker, J. H., Limburg, P. C., Nelis, G. F., & Kallenberg, C. G. M. (1998) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1998.00528.x · Cited by 91 · see citing works
Scharte, M., Han, X., Bertges, D. J., Fink, M. P., & Delude, R. L. (2003) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00076.2002 · Cited by 89 · see citing works
Agic, A., Djalali, S., Wolfler, M. M., Halis, G., Diedrich, K., & Hornung, D. (2008) · Reproductive Sciences · doi:10.1177/1933719108318598 · Cited by 88 · see citing works
Alpha-enolase: A novel cytosolic autoantigen in ANCA positive vasculitis
Moodie, F. D. L., Leaker, B. R., Cambridge, G., Totty, N. F., & Segal, A. W. (1993) · Kidney International · doi:10.1038/ki.1993.97 · Cited by 80 · 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-citationGitlits, V. M., Toh, B., & Sentry, J. W. (2001) · Journal of Investigative Medicine · doi:10.2310/6650.2001.34040 · Cited by 73 · see citing works
Circulating antibodies against α-enolase in patients with primary membranous nephropathy (MN)
Wakui, H., Imai, H., Komatsuda, A., & MIURA, A. B. (1999) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1999.01080.x · Cited by 67 · see citing works
Socolov, R. V., Buţureanu, S., Angioni, S. L., Sindilar, A., Boiculese, L. V., Cozma, L. G., & Socolov, D. G. (2010) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2010.10.008 · Cited by 65 · see citing works
Discovery of a novel biomarker in the urine in women with endometriosis
Tokushige, N., Markham, R., Crossett, B., Ahn, S. B., Nelaturi, V. L., Khan, A., & Fraser, I. S. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.05.016 · Cited by 61 · see citing works
Circulating cell-free DNA as a potential biomarker for minimal and mild endometriosis
Zachariah, R., Schmid, S., Radpour, R., Buerki, N., Fan, A. X.-C., Hahn, S., Holzgreve, W., & Zhong, X. Y. (2009) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60100-9 · Cited by 59 · see citing works
Chen, J., Xi, J., Tian, Y., Bova, G. S., & Zhang, H. (2013) · PROTEOMICS · doi:10.1002/pmic.201200541 · Cited by 55 · see citing works
Enolase and Arrestin are Novel Nonmyelin Autoantigens in Multiple Sclerosis
Forooghian, F., Cheung, R. K., Smith, W. C., O'Connor, P. W., & Dosch, H. (2007) · Journal of Clinical Immunology · doi:10.1007/s10875-007-9091-1 · Cited by 44 · see citing works
El-Kasti, M. M., Wright, C., Fye, H. K. S., Roseman, F., Kessler, B. M., & Becker, C. M. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.11.066 · Cited by 44 · see citing works
Secretion and excretion of human chorionic gonadotropin during early pregnancy
Lohstroh, P. N., Overstreet, J. W., Stewart, D. R., Nakajima, S. T., Cragun, J. R., Boyers, S. P., & Lasley, B. L. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2004.10.038 · Cited by 44 · see citing works
Bottini, P. V., Alves, M. A. V. F. R., & Garlipp, C. R. (2002) · American Journal of Kidney Diseases · doi:10.1053/ajkd.2002.29920 · Cited by 38 · see citing works
Walter, M., Berg, H., Leidenberger, F. A., Schweppe, K.-W., & Northemann, W. (1995) · Journal of Autoimmunity · doi:10.1016/s0896-8411(95)80027-1 · Cited by 36 · see citing works
Humoral Autoimmune Responses to the Squamous Cell Carcinoma Antigen Protein Family in Psoriasis
El-Rachkidy, R. G., Young, H. S., Griffiths, C. E. M., & Camp, R. D. R. (2008) · Journal of Investigative Dermatology · doi:10.1038/jid.2008.71 · Cited by 36 · see citing works
Identification of anti‐α‐enolase autoantibody as a novel serum marker for endometriosis
Nabeta, M., Abe, Y., Kagawa‐Miki, L., Haraguchi, R., Kito, K., Ueda, N., Sugita, A., Yokoyama, M., Kusanagi, Y., & Ito, M. (2009) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.200900055 · Cited by 32 · see citing works
Agic, A., Xu, H., Rehbein, M., Wölfler, M. M., Ebert, A. D., & Hornung, D. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.09.012 · Cited by 29 · see citing works
Wölfler, M. M., Meinhold-Heerlein, I. M., Söhngen, L., Rath, W. H., Knüchel, R., Neulen, J., Maass, N., & Henkel, C. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.03.061 · Cited by 23 · see citing works
Renigunta, A., Mutig, K., Rottermann, K., Schlichthörl, G., Preisig‐Müller, R., Daut, J., Waldegger, S., & Renigunta, V. (2011) · Cellular Physiology and Biochemistry · doi:10.1159/000335761 · Cited by 12 · see citing works
Langereis, J. D., Franciosi, L., Ulfman, L. H., & Koenderman, L. (2011) · Cytokine · doi:10.1016/j.cyto.2011.06.025 · Cited by 6 · see citing works
Flagged first, then by citations
1 of the 41 references couldn’t be matched to a known paper.
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Combination 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 227 · 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
“Despite elevation in women with endometriosis, enolase-1 lacked sufficient diagnostic power as an individual analyte (sensitivity 56% and specificity 72%) in a separate study [108].”
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 89 · see citing works
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 · see citing works
Pant, A., Moar, K., Arora, T. K., & Maurya, P. K. (2023) · Clinica Chimica Acta · doi:10.1016/j.cca.2023.117563 · Cited by 46 · see citing works
Current biomarkers for the detection of endometriosis
Tian, Z., Chang, X., Zhao, Y. P., & Zhu, H. (2020) · Chinese Medical Journal · doi:10.1097/cm9.0000000000001063 · Cited by 45 · see citing works
The diagnostic value of the combination of hemoglobin, CA199, CA125, and HE4 in endometriosis
Chen, T., Wei, J., Leng, T., Gao, F., & Hou, S. (2021) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.23947 · Cited by 43 · see citing works
The Diagnostic Accuracy of Combined Enolase/Cr, CA125, and CA19‐9 in the Detection of Endometriosis
Rokhgireh, S., Mehdizadehkashi, A., Chaichian, S., Delbandi, A., Allahqoli, L., Ahmadi-Pishkuhi, M., Khodaverdi, S., & Alkatout, İ. (2020) · BioMed Research International · doi:10.1155/2020/5208279 · Cited by 36 · see citing works
Williams, K. E., Miroshnychenko, O., Johansen, E. B., Niles, R. K., Sundaram, R., Kannan, K., Albertolle, M. E., Zhou, Y., Prasad, N., Drake, P. M., et al. (2014) · Journal of Proteomics · doi:10.1016/j.jprot.2014.09.015 · Cited by 30 · see citing works
Tabatabaei, F., Tahernia, H., Ghaedi, A., Bazrgar, A., & Khanzadeh, S. (2023) · BMC Women s Health · doi:10.1186/s12905-023-02692-7 · Cited by 26 · see citing works
Urinary Biomarkers for Detection of Clinical Endometriosis or Adenomyosis
Chen, W., Cheng, C., Liao, W., & Chang, T. (2022) · Biomedicines · doi:10.3390/biomedicines10040833 · Cited by 21 · see citing works
Dolińska, W., Draper, H., Othman, L., Thompson, C., Girvan, S., Cunningham, K., Allen, J., Rigby, A. S., Phillips, K., & Guinn, B. (2022) · F&S Reviews · doi:10.1016/j.xfnr.2022.12.001 · Cited by 21 · see citing works
Mezhlumova, N. A., Bobrov, М. Y., & Adamyan, L. V. (2018) · Russian Journal of Human Reproduction · doi:10.17116/repro201824061139 · Cited by 9 · see citing works
Biomarkers of endometriosis - current trends
Adamyan, L. V., & Aznaurova, Y. B. (2018) · Russian Journal of Human Reproduction · doi:10.17116/repro201824157-62 · Cited by 7 · see citing works
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Endometriosis Biomarkers in Body Fluids
Dakubo, G. D. (2016) · Springer eBooks · doi:10.1007/978-3-319-48360-3_14 · Cited by 1 · see citing works
Biomarkers in endometriosis-associated pain
Margatho, D., & Bahamondes, L. G. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-818988-7.00036-4
- Authors
- Yun, B. H., Lee, Y. S., Chon, S. J., Jung, Y. S., Yim, S. Y., Kim, H. Y., Park, J. H., Seo, S. K., Cho, S., Choi, Y. S., & Lee, B. S.
- Affiliations
- Yonsei University (KR)
- Corresponding author
- Cho, SiHyun
- ORCID
- Venue
- Biomarkers
- Publisher
- Informa UK Limited
- Published
- 2013-11-28
- Volume
- 19
- Issue
- 1
- Pages
- 16-21
- ISSN
- 1354-750X (ISSN-L)
- 1366-5804
- OpenAlex
- W2050558848
- Cited by
- 17
- References
- 41
- Citations by year
- 2024: 1 · 2023: 2 · 2022: 2 · 2021: 3 · 2020: 2 · 2018: 2 · 2016: 2 · 2015: 2 · 2014: 1
- FWCI
- 2.01
- Type
- journal article
- Language
- en
- Open access
- Licence
- cc-by-nc-nd
- Locations
- Biomarkers (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 › Surgery › Diagnosis and treatment of tuberculosis
- Keywords
- endometriosis, CA125, diagnostic accuracy, serum biomarkers, urinary biomarkers
- MeSH terms
- Adult, Creatinine, DNA-Binding Proteins, Endometriosis, Female, Humans, Phosphopyruvate Hydratase, ROC Curve, Biomarkers, Tumor, Biomarkers, Case-Control Studies, CA-125 Antigen, Tumor Suppressor Proteins
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