The DOI matches its Crossref record; 42 of the 42 references it cites were found in a registry or an index.
Discovery of phosphatidylcholines and sphingomyelins as biomarkers for ovarian endometriosis
Open accessAbstract
BACKGROUND: Current non-invasive diagnostic methods for endometriosis lack sensitivity and specificity. In search for new diagnostic biomarkers for ovarian endometriosis, we used a hypothesis-generating targeted metabolomics approach. METHODS: In a case-control study, we collected plasma of study participants and analysed their metabolic profiles. We selected a group of 40 patients with ovarian endometriosis who underwent laparoscopic surgery and a control group of 52 healthy women who underwent sterilization at the University Clinical Centre Ljubljana, Slovenia. Over 140 targeted analytes included glycerophospholipids, sphingolipids and acylcarnitines. The analytes were quantified by electrospray ionization tandem mass spectrometry. For assessing the strength of association between the metabolite or metabolite ratios and the disease, we used crude and adjusted odds ratios. A stepwise logistic regression procedure was used for selecting the best combination of biomarkers. RESULTS: Eight lipid metabolites were identified as endometriosis-associated biomarkers due to elevated levels in patients compared with controls. A model containing hydroxysphingomyelin SMOH C16:1 and the ratio between phosphatidylcholine PCaa C36:2 to ether-phospholipid PCae C34:2, adjusted for the effect of age and the BMI, resulted in a sensitivity of 90.0%, a specificity of 84.3% and a ratio of the positive likelihood ratio to the negative likelihood ratio of 48.3. CONCLUSIONS: Our results suggest that endometriosis is associated with elevated levels of sphingomyelins and phosphatidylcholines, which might contribute to the suppression of apoptosis and affect lipid-associated signalling pathways. Our findings suggest novel potential routes for therapy by specifically blocking highly up-regulated isoforms of phosphpolipase A2 and lysophosphatidylcholine acyltransferase 4.
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
“In a study comprising patients with ovarian endometriosis (n = 40), eight metabolites and 81 metabolite ratios were significantly higher in the endometriosis group compared with healthy controls undergoing laparoscopy for sterilization (n = 52) [93].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [93]
In the citing paper
“The combination of hydroxysphingomyelin C16:1 and the ratio between phosphatidylcholine C36:2 to ether-phospholipid C34:2, adjusted for the effect of age and BMI, provided a sensitivity of 90.0% and a specificity of 84.3% for the detection of endometriosis [93].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [93]
Citations
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232
HMDB: the Human Metabolome Database
Wishart, D. S., Tzur, D., Knox, C., Eisner, R., Guo, A. C., Young, N., Cheng, D., Jewell, K., Arndt, D., Sawhney, S., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkl923 · Cited by 3,219
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166
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
HMDB: a knowledgebase for the human metabolome
Wishart, D. S., Knox, C., Guo, A. C., Eisner, R., Young, N., Gautam, B., Hau, D., Psychogios, N., Dong, E., Bouatra, S., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn810 · Cited by 1,874
Update of the LIPID MAPS comprehensive classification system for lipids
Fahy, E., Subramaniam, S., Murphy, R. C., Nishijima, M., Raetz, C. R. H., Shimizu, T., Spener, F., van Meer, G., Wakelam, M. J. O., & Dennis, E. A. (2009) · Journal of Lipid Research · doi:10.1194/jlr.r800095-jlr200 · Cited by 1,628
PubChem: Integrated Platform of Small Molecules and Biological Activities
Bolton, E., Wang, Y., Thiessen, P. A., & Bryant, S. H. (2008) · Annual reports in computational chemistry · doi:10.1016/s1574-1400(08)00012-1 · Cited by 1,267
Platelet-Activating Factor and Related Lipid Mediators
Prescott, S. M., Zimmerman, G. A., Stafforini, D. M., & McIntyre, T. M. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.419 · Cited by 747
Genetics meets metabolomics: a genome-wide association study of metabolite profiles in human serum
Gieger, C., Geistlinger, L., Altmaier, E., Hrabé de Angelis, M., Kronenberg, F., Meitinger, T., Mewes, H.-W., Wichmann, H.-E., Weinberger, K. M., Adamski, J., et al. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000282 · Cited by 737
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Items 101–143 of 143
Biomarkers for Diagnosis of Pre-Eclampsia and Endometriosis
Wahid, B., Rafique, S., Ali, A., Waqar, M., Nabi, G., Wasim, M., & Idrees, M. (2018) · Biomarkers in Medicine · doi:10.2217/bmm-2018-0058 · Cited by 4
Biomarkers of endometriosis: How far have we come and where are we going?
Janša, V., Osredkar, J., Bokal, E. V., Rižner, T. L., & Frangež, H. B. (2021) · Slovenian Medical Journal · doi:10.6016/zdravvestn.3056 · Cited by 3
Self-citationLokhov, P. G., Maslov, D. L., Balashova, E. E., Trifonova, O. P., Medvedeva, N. V., Torkhovskaya, T. I., Ipatova, O. M., Archakov, A. I., Прокопьевич, М. П., Kukharchuk, V. V., et al. (2015) · Biochemistry (Moscow) Supplement Series B Biomedical Chemistry · doi:10.1134/s1990750815020109 · Cited by 4
Skeletal Muscle Metabolomics for Metabolic Phenotyping and Biomarker Discovery
Dyar, K. A., Artati, A., Cecil, A., & Adamski, J. (2019) · Springer eBooks · doi:10.1007/978-1-4939-9802-9_10 · Cited by 4
Self-citationYang, H. (2024) · Polish Journal of Microbiology · doi:10.33073/pjm-2024-041 · Cited by 3
Metabolite changes in patients with endometriosis: new potential diagnostic and therapeutic targets
Chang, L.-Y., Hou, X., Li, D., & Wang, X.-Q. (2025) · Reproductive and Developmental Medicine · doi:10.1097/rd9.0000000000000122 · Cited by 5
Metabolomics: the perspective search of methods to overcome infertility
Kalinina, E. A., Викторович, М. А., Зубарева, Т. М., Sitkin, S. I., Dedul, A. G., Sheveleva, T. S., Гамзатова, З. Х., Bejenar, V. F., & Komlichenko, E. V. (2015) · Gynecological Endocrinology · doi:10.3109/09513590.2015.1086515 · Cited by 3
Zhang, X., Zhang, L., Wang, Q., Sun, X., Yang, D., Xing, Y., & Ma, X. (2019) · Journal of Traditional Chinese Medical Sciences · doi:10.1016/j.jtcms.2019.11.005 · Cited by 3
Detection and Distribution of Sphingolipids in Tissue by FTICR MALDI-Imaging Mass Spectrometry
Jones, E. E., Dworski, S., Kamani, M., Canals, D., Wada, M., Liu, X., Hannun, Y. A., Norris, J. S., Medin, J. A., & Drake, R. R. (2015) · Springer eBooks · doi:10.1007/978-3-319-20750-6_15 · Cited by 3
The diagnosis of endometriosis with the help of mass spectrometry (a review)
Borisova, A. V., Kozachenko, K. A. V., Starodubtseva, N. L., Бугрова, А. Е., Евгеньевич, Ф. В., & Adamjan, L. V. (2015) · Russian Journal of Human Reproduction · doi:10.17116/repro201521659-68 · Cited by 3
Metabolomics for improving pregnancy outcomes in women undergoing assisted reproductive technologies
Siristatidis, C. S., Vogiatzi, P., Varounis, C., Vaidakis, D., & Trivella, M. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd011872 · Cited by 3
Pergialiotis, V., Zarkadoulas, N., Goula, K., Frountzas, M., Antoniadou, F., Dimitroulis, D., Vlachos, D., Papapanagiotou, A., Verikokos, C., Perrea, D. N., et al. (2022) · Cureus · doi:10.7759/cureus.30290 · Cited by 2
Liu, L., Yin, J., Liu, Y., Li, B., Kang, S., & Du, N. (2024) · Medicine · doi:10.1097/md.0000000000040690 · Cited by 2
Wu, X., Yu, X., Lu, Y., Xie, A., Su, Y., Zhang, L., Lin, Y., & Gan, X. (2025) · Journal of Multidisciplinary Healthcare · doi:10.2147/jmdh.s527221 · Cited by 2
Peripheral Blood Biomarkers for Endometriosis
Fassbender, A., Dorien, O., Becker, C. M., & D’Hooghe, T. M. (2017) · Springer eBooks · doi:10.1007/978-3-319-59856-7_7 · Cited by 2
Nisenblat, V., & Hull, M. L. (2018) · Springer eBooks · doi:10.1007/978-3-319-71138-6_16 · Cited by 2
Liang, Q., Wang, G., Chen, X., Li, Q., Chen, F., Liu, W., Wang, D., Xu, H., Zi-qiang, Q., & Li, D. (2025) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2025.104861 · Cited by 1
Endometriosis Biomarkers in Body Fluids
Dakubo, G. D. (2016) · Springer eBooks · doi:10.1007/978-3-319-48360-3_14 · Cited by 1
Detection of Aristaless-related homeobox protein in ovarian sex cord-stromal tumors
Knific, T., Grazio, S. F., & Rižner, T. L. (2017) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2017.12.005 · Cited by 1
Self-citationHarnessing the Potential of Metabolomic Biomarkers for Metabolic Health
Gupta, S. G., Kaur, P., Kaur, R., & Singh, T. G. (2024) · Advances in bioinformatics and biomedical engineering book series · doi:10.4018/979-8-3693-1922-2.ch007 · Cited by 1
Metabolomics as a Candidate for Endometriosis Biomarker: A Systematic Review
Meidyana, S., & Fedora, K. (2024) · Fertility & Reproduction · doi:10.1142/s2661318224500075 · Cited by 1
Endometriosis Research: From Bench to Bedside
Laganà, A. S., & La Rosa, V. L. (2022) · MDPI eBooks · doi:10.3390/books978-3-0365-2798-7
Follicular fluid metabolomic analysis in women with Hashimoto’s thyroiditisPreprint
Bastos, D. C. D. S., Chiamolera, M. I., Silva, R. E. C., de Souza, M. D. C. B., Antunes, R. D. A., de Souza, M. M., Mancebo, A. C. A., Arêas, P. C. F., dos Reis, F. M., Turco, E. G. L., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.19.520992
Endometriosis: Pathogenesis, Diagnosis and Treatment, volume II
(2024) · Frontiers research topics · doi:10.3389/978-2-8325-4894-3
Growth Arrest-Specific Protein 6 Is Elevated in Endometriosis but Shows Poor Diagnostic Performance
Pušić, M. N., Marijan, R., Klančič, T., Knific, T., Frangež, H. B., & Rižner, T. L. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26178348
Self-citationJing, W., Wei, C., & Pang, L. (2025) · BMC Women s Health · doi:10.1186/s12905-025-04130-2
Wang, J., Zheng, W., Zhang, S., Yan, K., Jin, M., Hu, H., Ma, Z., Gong, F., Lu, G., Ren, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16599467
Wang, J., Zheng, W., Zhang, S., Yan, K., Jin, M., Hu, H., Ma, Z., Gong, F., Lu, G., Ren, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16599479
Wang, J., Zheng, W., Zhang, S., Yan, K., Jin, M., Hu, H., Ma, Z., Gong, F., Lu, G., Ren, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16599476
Wang, J., Zheng, W., Zhang, S., Yan, K., Jin, M., Hu, H., Ma, Z., Gong, F., Lu, G., Ren, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16599473
Wang, J., Zheng, W., Zhang, S., Yan, K., Jin, M., Hu, H., Ma, Z., Gong, F., Lu, G., Ren, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16599485
Wang, J., Zheng, W., Zhang, S., Yan, K., Jin, M., Hu, H., Ma, Z., Gong, F., Lu, G., Ren, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16599482
Wang, J., Zheng, W., Zhang, S., Yan, K., Jin, M., Hu, H., Ma, Z., Gong, F., Lu, G., Ren, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16599470
YuHan, D. U. A. N., HeLin, W. A. N. G., & ZHANG, K. (2025) · Scientia Sinica Vitae · doi:10.1360/ssv-2024-0352
Transcriptome profiling to identify blood biomarkers for peritoneal endometriosisPreprint
Pušić, M. N., Vižintin, A., Režen, T., Frangež, H. B., Wenzl, R. J., & Rižner, T. L. (2025) · medRxiv · doi:10.64898/2025.12.23.25342915
Self-citationOlcha, P., Kępski, M., Paja, W., Baran, M., Adamczuk, K., Świerszcz, Ł., Gałczyński, K., & Depciuch, J. (2026) · Microchemical Journal · doi:10.1016/j.microc.2026.118821
Cecil, A., Vouk, K., Pušić, M. N., Vogler, A., Wenzl, R. J., Prehn, C. P., Adamski, J., & Rižner, T. L. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.05.736551
Self-citationMachado, M. (2026) · Advanced Science · doi:10.1002/advs.202521907
Gut commensal Olsenella profusa promotes endometriosis via lysophosphatidylcholine metabolite
Chen, Y., Zhou, Z., Huang, B., Xie, X., Cao, Y., Zeng, S., Li, B., Xia, F., Peng, L., Liang, J., et al. (2026) · Cell Reports Medicine · doi:10.1016/j.xcrm.2026.102970
Multi-omics profiling identifies an immunometabolic signature associated with endometriosis
Pan, W., Lyu, G., Wang, Y., Chen, T., Liu, S., Fan, X., Liu, R., Lin, H., Li, G., Su, X., et al. (2026) · Frontiers in Endocrinology · doi:10.3389/fendo.2026.1912463
Mei, S., Ding, N., Cheng, M., Zhang, C., Miao, J., Liu, M., Shi, X., & Wang, X. (2026) · Molecular Human Reproduction · doi:10.1093/molehr/gaag047
Liao, Y., Shi, Y., Pang, X., Yang, Y., Chen, X., Tang, Z., Xie, P., & Cao, X. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1924352
Metadata
- Authors
- Vouk, K., Hevir, N., Ribič-Pucelj, M., Haarpaintner, G., Scherb, H., Osredkar, J., Möller, G., Prehn, C., Rižner, T. L., & Adamski, J.
- Affiliations
- University of Ljubljana (SI)
- Ljubljana University Medical Centre (SI)
- Helmholtz Munich (DE)
- Corresponding author
- Rižner, T. Lanišnik
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-08-01
- Volume
- 27
- Issue
- 10
- Pages
- 2955-2965
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2129793603
- Cited by
- 143
- References
- 42
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 12 · 2023: 8 · 2022: 10 · 2021: 16 · 2020: 8 · 2019: 7 · 2018: 11 · 2017: 18 · 2016: 9 · 2015: 15 · 2014: 6 · 2013: 2
- FWCI
- 8.57
- Type
- journal article
- Language
- en
- Open access
- Licence
- other-oa
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Repository of the University of Ljubljana (University of Ljubljana) (publishedVersion, other-oa)
- Site cant be reached (submittedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Keywords
- endometrioma, phosphatidylcholine, sphingomyelin, plasma lipid biomarkers, targeted metabolomics, non-invasive diagnosis, glycerophospholipids, sphingolipids, acylcarnitines, apoptosis, phospholipase A2
- MeSH terms
- Adult, Age Factors, Endometriosis, Female, Humans, Phosphatidylcholines, Sensitivity and Specificity, Sphingomyelins, Biomarkers, Body Mass Index, Likelihood Functions, Logistic Models, Case-Control Studies
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
