Cited by 143Endometriosis Research and TreatmentMetabolomics and Mass Spectrometry StudiesOvarian function and disorders

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 access

Vouk, K., Hevir, N., Ribič-Pucelj, M., Haarpaintner, G., Scherb, H., Osredkar, J., Möller, G., Prehn, C., Rižner, T. Lanišnik, Adamski, J.·2012·Human Reproduction

DOI 10.1093/humrep/des152

Open this paper in CoChat — free account

Abstract

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.

Integrity signals

Registry

Crossref · 10.1093/humrep/des152

Cites

42 of 42 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

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
Endometriosis
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

Show all 42 references

Sorted by citations

Blood 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
Metabolomics for clinical use and research in chronic kidney disease
Hocher, B., & Adamski, J. (2017) · Nature Reviews Nephrology · doi:10.1038/nrneph.2017.30 · Cited by 339
Self-citation
Metabolomics for Biomarker Discovery: Moving to the Clinic
Zhang, A., Sun, H. J., Yan, G., Wang, P., & Wang, X. (2015) · BioMed Research International · doi:10.1155/2015/354671 · Cited by 293
Higher plasma levels of lysophosphatidylcholine 18:0 are related to a lower risk of common cancers in a prospective metabolomics study
Kuhn, T. E., Floegel, A., Sookthai, D., Johnson, T., Rolle-Kampczyk, U. E., Otto, W., von Bergen�, M., Boeing, H., & Kaaks, R. (2016) · BMC Medicine · doi:10.1186/s12916-016-0552-3 · Cited by 247
Biomarkers 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
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
“roscopy for sterilization (n = 52) [93].”
Metabolomics for the masses: The future of metabolomics in a personalized world
Trivedi, D. K., Hollywood, K. A., & Goodacre, R. (2017) · European Journal of Molecular & Clinical Medicine · doi:10.1016/j.nhtm.2017.06.001 · Cited by 201
Mass spectrometry‐based metabolomics: applications to biomarker and metabolic pathway research
Zhang, A., Sun, H. J., Yan, G., Wang, P., & Wang, X. (2015) · Biomedical Chromatography · doi:10.1002/bmc.3453 · Cited by 197
Plasma and Serum Lipidomics of Healthy White Adults Shows Characteristic Profiles by Subjects’ Gender and Age
Ishikawa, M., Maekawa, K., Saito, K., Senoo, Y., Urata, M., Murayama, M., Tajima, Y., Kumagai, Y., & Saito, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091806 · Cited by 188
Guidelines for the design, analysis and interpretation of ‘omics’ data: focus on human endometrium
Altmäe, S., Esteban, F. J., Stavreus-Evers, A., Simón, C., Giudice, L., Lessey, B. A., Horcajadas, J. A., Macklon, N. S., D'Hooghe, T., Campoy, C., et al. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmt048 · Cited by 151
Targeted Metabolomics of Dried Blood Spot Extracts
Zukunft, S., Sorgenfrei, M., Prehn, C. P., Möller, G., & Adamski, J. (2013) · Chromatographia · doi:10.1007/s10337-013-2429-3 · Cited by 100
Self-citation
Direct Infusion Mass Spectrometry for Metabolomic Phenotyping of Diseases
González‐Domínguez, R., Sayago, A., & Fernández‐Recamales, Á. (2016) · Bioanalysis · doi:10.4155/bio-2016-0202 · Cited by 100
AQuA: An Automated Quantification Algorithm for High-Throughput NMR-Based Metabolomics and Its Application in Human Plasma
Röhnisch, H. E., Eriksson, J. W., Müllner, E., Agback, P., Sandström, C., & Moazzami, A. A. (2017) · Analytical Chemistry · doi:10.1021/acs.analchem.7b04324 · Cited by 97
Altered levels of acylcarnitines, phosphatidylcholines, and sphingomyelins in peritoneal fluid from ovarian endometriosis patients
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
Self-citation
Dysregulated Sphingolipid Metabolism in Endometriosis
Lee, Y. H., Tan, C. W., Venkatratnam, A., Tan, C. S., Liang, C., Loh, S. F., Griffith, L. G., Tannenbaum, S. R., & Chan, J. K. Y. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-1340 · Cited by 83
Factors affecting longitudinal trajectories of plasma sphingomyelins: the Baltimore Longitudinal Study of Aging
Mielke, M. M., Bandaru, V. V. R., Han, D., An, Y., Resnick, S. M., Ferrucci, L., & Haughey, N. J. (2014) · Aging Cell · doi:10.1111/acel.12275 · Cited by 78
Lipidomics analysis of follicular fluid by ESI-MS reveals potential biomarkers for ovarian endometriosis
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
On-Tissue Localization of Ceramides and Other Sphingolipids by MALDI Mass Spectrometry Imaging
Jones, E. E., Dworski, S., Canals, D., Casas, J., Fabriàs, G., Schoenling, D., Levade, T., Denlinger, C. E., Hannun, Y. A., Medin, J. A., et al. (2014) · Analytical Chemistry · doi:10.1021/ac501937d · Cited by 75
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
Discovery of Phosphatidic Acid, Phosphatidylcholine, and Phosphatidylserine as Biomarkers for Early Diagnosis of Endometriosis
Li, J., Gao, Y., Guan, L., Zhang, H., Sun, J., Gong, X., Li, D., Chen, P., Ma, Z., Liang, X., et al. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00014 · Cited by 68
Metabolomic profiling and biochemical evaluation of the follicular fluid of endometriosis patients
Santonastaso, M., Pucciarelli, A., Costantini, S., Caprio, F., Sorice, A., Capone, F., Antonella, N., Iardino, P., Colacurci, N., & Emilio, C. (2017) · Molecular BioSystems · doi:10.1039/c7mb00181a · Cited by 65
Associations between persistent organic pollutants and endometriosis: A multiblock approach integrating metabolic and cytokine profiling
Matta, K., Lefebvre, T., Vigneau, É., Cariou, V., Marchand, P., Guitton, Y., Royer, A., Ploteau, S., Bizec, B. L., Antignac, J., et al. (2021) · Environment International · doi:10.1016/j.envint.2021.106926 · Cited by 62
The association of body mass index with endometriosis and disease severity in women with pain
Holdsworth‐Carson, S. J., Dior, U. P., Colgrave, E. M., Healey, M., Montgomery, G. W., Rogers, P. A. W., & Girling, J. E. (2018) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.1177/2284026518773939 · Cited by 59
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
Metabolomics Reveals Altered Lipid Metabolism in a Mouse Model of Endometriosis
Dutta, M., Anitha, M., Smith, P. B. W., Chiaro, C. R., Maan, M., Chaudhury, K., & Patterson, A. D. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00197 · Cited by 56
Molecular signatures of ovarian diseases: Insights from network medicine perspective
Kori, M., Göv, E., & Arğa, K. Y. (2016) · Systems Biology in Reproductive Medicine · doi:10.1080/19396368.2016.1197982 · Cited by 58
De novo synthesis of sphingolipids is essential for decidualization in mice
Ding, N., Qi, Q.-R., Gu, X., Zuo, R.-J., Liu, J., & Yang, Z. (2017) · Theriogenology · doi:10.1016/j.theriogenology.2017.09.036 · Cited by 53
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
Self-citation
Endometriosis research in the -omics era
Goulielmos, G. N., Matalliotakis, M., Matalliotaki, C., Eliopoulos, E., Matalliotakis, I., & Zervou, M. I. (2020) · Gene · doi:10.1016/j.gene.2020.144545 · Cited by 50
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
Pathophysiologic processes have an impact on the plasma metabolomic signature of endometriosis patients
Vicente-Muñoz, S., Morcillo, I., Puchades‐Carrasco, L., Payá, V., Pellicer, A., & Pineda‐Lucena, A. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.09.014 · Cited by 47
Metabolomics in endometriosis: challenges and perspectives for future studies
Ortiz, C. N., Torres-Reverón, A., & Appleyard, C. B. (2021) · Reproduction and Fertility · doi:10.1530/raf-20-0047 · Cited by 50
Emerging hallmarks of endometriosis metabolism: A promising target for the treatment of endometriosis
Lu, J., Ling, X., Liu, L., Jiang, A., Ren, C., Lü, C., & Yu, Z. (2022) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2022.119381 · Cited by 48
Diagnostic potential of peritoneal fluid biomarkers of endometriosis
Rižner, T. L. (2015) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.2015.1015994 · Cited by 45
Self-citation
Endocrinology Meets Metabolomics: Achievements, Pitfalls, and Challenges
Tokarz, J., Haid, M., Cecil, A., Prehn, C. P., Artati, A., Möller, G., & Adamski, J. (2017) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2017.07.001 · Cited by 44
Self-citation
Direct Mass Spectrometry Differentiation of Ectopic and Eutopic Endometrium in Patients with Endometriosis
Adamyan, L. V., Starodubtseva, N. L., Borisova, A. V., Stepanian, A. A., Chagovets, V., Salimova, D., Wang, Z., Kononikhin, A. S., Popov, I. A., Bugrova, A. E., et al. (2017) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2017.08.658 · Cited by 43
The Relationship of Circular RNAs With Ovarian Endometriosis
Xu, X., Jia, S., Dai, Y., Zhang, J., Li, X., Shi, J., Leng, J., & Lang, J. (2018) · Reproductive Sciences · doi:10.1177/1933719118759439 · Cited by 40
Metabolomics for Diagnosis and Prognosis of Uterine Diseases? A Systematic Review
Tokarz, J., Adamski, J., & Rižner, T. L. (2020) · Journal of Personalized Medicine · doi:10.3390/jpm10040294 · Cited by 43
Self-citation
Integrative analysis of transcriptomic and metabolomic profiles reveals abnormal phosphatidylinositol metabolism in follicles from endometriosis‐associated infertility patients
Dai, Y., Lin, X., Liu, N., Shi, L., Zhuo, F., Huang, Q., Gu, W., Zhao, F., Zhang, Y., Zhang, Y., et al. (2023) · The Journal of Pathology · doi:10.1002/path.6079 · Cited by 40
Metabolomics for improving pregnancy outcomes in women undergoing assisted reproductive technologies
Siristatidis, C. S., Sertedaki, E., & Vaidakis, D. (2017) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd011872.pub2 · Cited by 36
Endometriosis foci differentiation by rapid lipid profiling using tissue spray ionization and high resolution mass spectrometry
Chagovets, V., Wang, Z., Kononikhin, A. S., Starodubtseva, N. L., Borisova, A. V., Salimova, D., Popov, I. A., Kozachenko, A. V., Chingin, K., Chen, H., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-02708-x · Cited by 34
Presurgical blood metabolites and risk of postsurgical pelvic pain in young patients with endometriosis
Sasamoto, N., Zeleznik, O. A., Vitonis, A. F., Missmer, S. A., Laufer, M. R., Ávila-Pacheco, J., Clish, C. B., & Terry, K. L. (2022) · Fertility and Sterility · doi:10.1016/j.fertnstert.2022.02.012 · Cited by 31
Metabolomics for improving pregnancy outcomes in women undergoing assisted reproductive technologies
Siristatidis, C. S., Sertedaki, E., Vaidakis, D., Varounis, C., & Trivella, M. (2018) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd011872.pub3 · Cited by 32
Elevated peritoneal fluid ceramides in human endometriosis-associated infertility and their effects on mouse oocyte maturation
Lee, Y. H., Yang, J. X., Allen, J. C., Tan, C. S., Chern, B. S. M., Tan, T. Y., Tan, H. H., Mattar, C. N. Z., & Chan, J. K. Y. (2018) · Fertility and Sterility · doi:10.1016/j.fertnstert.2018.05.003 · Cited by 30
Molecular Imaging of Endometriosis Tissues using Desorption Electrospray Ionization Mass Spectrometry
Feider, C. L., Woody, S., Ledet, S., Zhang, J., Sebastian, K., Breen, M., & Eberlin, L. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-51853-y · Cited by 29
Metabolomic biomarkers of endometriosis: A systematic review
Adamyan, L. V., Pivazyan, L. G., Zarova, E., Avetisyan, J. S., Laevskaya, A., Sarkisova, A., & Stepanian, A. A. (2024) · Journal of Endometriosis and Uterine Disorders · doi:10.1016/j.jeud.2024.100077 · Cited by 27
Dysregulated sphingolipid metabolism and autophagy in granulosa cells of women with endometriosis
Turathum, B., Gao, E.-M., Grataitong, K., Liu, Y., Wang, L., Dai, X., & Chian, R. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.906570 · Cited by 26
Lipidomic Alterations and PPARα Activation Induced by Resveratrol Lead to Reduction in Lesion Size in Endometriosis Models
Chen, Z., Wang, C., Lin, C., Zhang, L., Zheng, H., Zhou, Y., Li, X., Li, C., Zhang, X., Yang, X., et al. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/9979953 · Cited by 25
Endometrial whole metabolome profile at the receptive phase: influence of Mediterranean Diet and infertility
Molina, N. M., Jurado‐Fasoli, L., Sola‐Leyva, A., Sevilla-Lorente, R., Canha-Gouveia, A., Ruíz-Durán, S., Fontes, J., Aguilera, C. M., & Altmäe, S. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1120988 · Cited by 25
TGFBI as a candidate biomarker for non-invasive diagnosis of early-stage endometriosis
Janša, V., Pušić, M. N., Frangež, H. B., & Rižner, T. L. (2023) · Human Reproduction · doi:10.1093/humrep/dead091 · Cited by 29
Self-citation
A mass spectrometric insight into the origins of benign gynecological disorders
Yang, H., Lau, W. B., Lau, B., Yu, X., Zhou, S., Zhao, L., Luo, Z., Lin, Q., Ren, N., Zhao, X., et al. (2015) · Mass Spectrometry Reviews · doi:10.1002/mas.21484 · Cited by 25
Serum metabolic profiling study of endometriosis by using wooden-tip electrospray ionization mass spectrometry
Yang, B., Liu, F., Wang, L., Zou, Y., Wang, F., Deng, W., Wan, X., Yang, X., He, M. L., & Huang, O. (2015) · Analytical Methods · doi:10.1039/c5ay01312g · Cited by 24
Serum untargeted metabolomics delineates the metabolic status in different subtypes of non-alcoholic fatty liver disease
Liu, L., Zhao, J., Zhang, R., Wang, X., Wang, Y., Chen, Y., & Feng, R. (2021) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2021.114058 · Cited by 24
Aging-related Changes in Mouse Serum Glycerophospholipid Profiles
Kim, S., Cheon, H., Song, J.-C., Yun, S., Park, S. I., & Jeon, J. (2014) · Osong Public Health and Research Perspectives · doi:10.1016/j.phrp.2014.10.002 · Cited by 24
Association between Perfluorooctanoic Acid–Related Poor Embryo Quality and Metabolite Alterations in Human Follicular Fluid during IVF: A Cohort Study
Xu, J., Wang, Q., Jiao, X., Kong, P., Chen, S., Yang, W., Liu, W., Li, K., Teng, X., & Guo, Y. (2025) · Environmental Health Perspectives · doi:10.1289/ehp15422 · Cited by 23
Circadian Time Structure of Circulating Plasma Lipid Components in Healthy Indians of Different Age Groups
Singh, R., Sharma, S., Singh, R. K., & Cornélissen, G. (2015) · Indian Journal of Clinical Biochemistry · doi:10.1007/s12291-015-0519-8 · Cited by 23
Follicular Fluid and Blood Monitorization of Infertility Biomarkers in Women with Endometriosis
Brinca, A. T., Peiró, A. M., Matallı́n, P., Buendicho, I. E., Oliani, A. H., Silva, V., Vicente, L. F., Ramalhinho, A. C., & Gallardo, E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25137177 · Cited by 23
Identification of potential endometriosis biomarkers in peritoneal fluid and blood plasma via shotgun lipidomics
Starodubtseva, N. L., Chagovets, V., Borisova, A. V., Salimova, D., Aleksandrova, N. V., Chingin, K., Chen, H., & Евгеньевич, Ф. В. (2019) · Clinical mass spectrometry · doi:10.1016/j.clinms.2019.05.007 · Cited by 21
Metabolomics in Central Sensitivity Syndromes
Miller, J. S., RODRIGUEZ‐SAONA, L. E., & Hackshaw, K. V. (2020) · Metabolites · doi:10.3390/metabo10040164 · Cited by 22
Comparison of circulating lipid profiles between fasting humans and three animal species used in preclinical studies: mice, rats and rabbits
Ishikawa, M., Saito, K., Urata, M., Kumagai, Y., Maekawa, K., & Saito, Y. (2015) · Lipids in Health and Disease · doi:10.1186/s12944-015-0104-4 · Cited by 20
A Comparison of Tissue Spray and Lipid Extract Direct Injection Electrospray Ionization Mass Spectrometry for the Differentiation of Eutopic and Ectopic Endometrial Tissues
Chagovets, V., Wang, Z., Kononikhin, A. S., Starodubtseva, N. L., Borisova, A. V., Salimova, D., Popov, I. A., Kozachenko, A. V., Chingin, K., Chen, H., et al. (2017) · Journal of the American Society for Mass Spectrometry · doi:10.1007/s13361-017-1792-y · Cited by 20
Decreased Serum Levels of Sphingomyelins and Ceramides in Sickle Cell Disease Patients
Aslan, M., Kıraç, E., Kaya, S., Özcan, F., Salim, O., & Küpesiz, O. A. (2018) · Lipids · doi:10.1002/lipd.12027 · Cited by 22
Recent progress in metabolomics for analyzing common infertility conditions that affect ovarian function
Kobayashi, H., & Imanaka, S. (2024) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12609 · Cited by 19
Metabolomics for the identification of biomarkers in endometriosis
Pandey, S. (2024) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-024-07796-5 · Cited by 19
Metabolomic profile as a noninvasive adjunct tool for the diagnosis of Grades III and IV endometriosis‐related infertility
Braga, D. P. A. F., Montani, D. A., Setti, A. S., Turco, E. G. L., Oliveira‐Silva, D., & Borges, E. (2019) · Molecular Reproduction and Development · doi:10.1002/mrd.23221 · Cited by 21
Association of endocannabinoids with pain in endometriosis
Andrieu, T., Chicca, A., Pellegata, D., Bersinger, N. A., Imboden, S., Nirgianakis, K., Gertsch, J., & Mueller, M. D. (2021) · Pain · doi:10.1097/j.pain.0000000000002333 · Cited by 18
Is there a role for small molecule metabolite biomarkers in the development of a diagnostic test for endometriosis?
Tomkins, N. E., Girling, J. E., Boughton, B. A., & Holdsworth‐Carson, S. J. (2022) · Systems Biology in Reproductive Medicine · doi:10.1080/19396368.2022.2027045 · Cited by 17
Metabolomic analysis of follicular fluid from women with Hashimoto thyroiditis
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. (2023) · Scientific Reports · doi:10.1038/s41598-023-39514-7 · Cited by 17
Mass spectrometry analysis of blood plasma lipidome as method of disease diagnostics, evuation of effectiveness and optimization of drug therapy
Lokhov, 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) · Biomeditsinskaya Khimiya · doi:10.18097/pbmc20156101007 · Cited by 17
Feature selection for OPLS discriminant analysis of cancer tissue lipidomics data
Tokareva, A., Chagovets, V., Starodubtseva, N. L., Мирзоевна, Н. Н., Nekrasova, M. E., Kononikhin, A. S., Евгеньевич, Ф. В., Николаев, Е. Н., & Sukhikh, G. T. (2019) · Journal of Mass Spectrometry · doi:10.1002/jms.4457 · Cited by 17
Diagnostic Value of Menstrual Blood Lipidomics in Endometriosis: A Pilot Study
Starodubtseva, N. L., Chagovets, V., Tokareva, A., Равилевна, Д. М., Kukaev, E., Novoselova, A., Евгеньевич, Ф. В., Pavlovich, S. V., & Sukhikh, G. T. (2024) · Biomolecules · doi:10.3390/biom14080899 · Cited by 21
Circulating estradiol and its biologically active metabolites in endometriosis and in relation to pain symptoms
Émond, J.-P., Caron, P., Pušić, M. N., Turcotte, V., Simonyan, D., Vogler, A., Osredkar, J., Rižner, T. L., & Guillemette, C. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1034614 · Cited by 18
Self-citation
Histone lactylation-mediated overexpression of RASD2 promotes endometriosis progression via upregulating the SUMOylation of CTPS1
Wang, Z., Mao, Y., Wang, Z., Li, S., Hong, Z., Zhou, R., Xu, S., Xiong, Y., & Zhang, Y. (2024) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00493.2024 · Cited by 14
Clinical picture and diagnosis of genital endometriosis
Yarmolinskaya, M. I., Rusina, E. I., Khachaturyan, A. R., & Florova, M. S. (2016) · Journal of obstetrics and women s diseases · doi:10.17816/jowd6554-21 · Cited by 16
Comparative metabolomic profiling of women undergoing in vitro fertilization procedures reveals potential infertility-related biomarkers in follicular fluid
Dabaja, M. Z., dos Santos, A. A., Christofolini, D. M., Barbosa, C. P., de Oliveira, D. N., de Oliveira, A. N., Melo, C. F. O. R., Guerreiro, T. M., & Catharino, R. R. (2022) · Scientific Reports · doi:10.1038/s41598-022-24775-5 · Cited by 13
Lipid responses to environmental perfluoroalkyl substance exposure in a Taiwanese Child cohort
Lee, S.-H., Tseng, W.-C., Du, Z.-Y., Lin, W., Chen, M., Lin, C., Lien, G., Liang, H., Wen, H., Guo, Y. L., et al. (2021) · Environmental Pollution · doi:10.1016/j.envpol.2021.117007 · Cited by 13
Models Including Serum CA-125, BMI, Cyst Pathology, Dysmenorrhea or Dyspareunia for Diagnosis of Endometriosis
Knific, T., Vouk, K., Vogler, A., Osredkar, J., Gstoettner, M., Wenzl, R. J., & Rižner, T. L. (2018) · Biomarkers in Medicine · doi:10.2217/bmm-2017-0426 · Cited by 13
Self-citation
The Current Applications of Metabolomics in Understanding Endometriosis: A Systematic Review
Collie, B., Troisi, J., Lombardi, M., Symes, S. J. K., & Richards, S. M. (2025) · Metabolites · doi:10.3390/metabo15010050 · Cited by 17
Sphingomyelin is involved in multisite musculoskeletal pain: evidence from metabolomic analysis in 2 independent cohorts
Pan, F., Liu, M., Randell, E. W., Rahman, P., Jones, G., & Zhai, G. (2020) · Pain · doi:10.1097/j.pain.0000000000002163 · Cited by 11
An increase of phosphatidylcholines in follicular fluid implies attenuation of embryo quality on day 3 post-fertilization
Wang, J., Zheng, W., Zhang, S., Yan, K., Jin, M., Hu, H., Ma, Z., Gong, F., Lu, G., Ren, Y., et al. (2021) · BMC Biology · doi:10.1186/s12915-021-01118-w · Cited by 11
Metabolomic profiling in follicular fluid of patients with infertility-related deep endometriosis
Cordeiro, F. B., Cataldi, T. R., da Costa, L. D. V. T., de Souza, B. Z., Montani, D. A., Fraietta, R., Labate, C. A., Cedenho, A. P., & Turco, E. G. L. (2017) · Metabolomics · doi:10.1007/s11306-017-1262-3 · Cited by 11
Evaluating the association between lipidome and female reproductive diseases through comprehensive Mendelian randomization analyses
Ma, Y., Wu, F., Yu, Z., & Yang, L. (2025) · Scientific Reports · doi:10.1038/s41598-025-86794-2 · Cited by 12
Analysis of CARD10 and CARD11 somatic mutations in patients with ovarian endometriosis
Zou, Y., Zhou, J., Wang, F., Zhang, Z., Liu, F., Luo, Y., Tan, J., Zeng, X., Wan, X., & Huang, O. (2018) · Oncology Letters · doi:10.3892/ol.2018.8659 · Cited by 10
The metabolomic profile of endometrial receptivity in recurrent miscarriage
Craciunas, L., Chu, J., Pickering, O., Mohiyiddeen, L., & Coomarasamy, A. (2022) · Minerva Obstetrics and Gynecology · doi:10.23736/s2724-606x.22.05151-x · Cited by 9
Metabolomic Characteristics in Endometriosis Patients
Angioni, S. L., Saponara, S., Succu, A. G., Sigilli, M., Scicchitano, F., & D’Alterio, M. N. (2020) · ISGE series · doi:10.1007/978-3-030-57866-4_2 · Cited by 9
Metabolomic Biomarkers in Gynecology: A Treasure Path or a False Path?
Govorov, I., Sitkin, S. I., Pervunina, T. M., Moskvin, A., Baranenko, D., & Komlichenko, E. V. (2019) · Current Medicinal Chemistry · doi:10.2174/0929867326666190104124245 · Cited by 9
18F-Fluorocholine Uptake and Positron Emission Tomography Imaging in Rat Peritoneal Endometriosis
Silveira, M. B., Rodrigues, D. M., de Araújo, M. R., Santiago, M. A., Gonçalves, N. T., Schirmer, B. G. D. A., Carneiro, M. M., dos Reis, F. M., Malamut, C., & Ferreira, M. C. F. (2017) · Reproductive Sciences · doi:10.1177/1933719117728799 · Cited by 9
Metabolomics analysis in endometriosis patients: is it a step toward the future?
Angioni, S. L., Saponara, S., & Vitale, S. G. (2023) · Gynecological Endocrinology · doi:10.1080/09513590.2023.2227276 · Cited by 9
Metabolome analysis as a potential source of endometriosis biomarkers with the use of multiomics approach in its diagnosis
Wojtyła, C., Kupcewicz, B., Tołwiński, I., Samborowska, E., Radkiewicz, M., Jaźwiec, R., Sakowicz, A., Rubel, T., Goszczynska, A., Winogradska, B., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-22598-8 · Cited by 9
A comprehensive multiplatform metabolomic analysis reveals alterations of 2-hydroxybutyric acid among women with deep endometriosis related to the pesticide trans-nonachlor
Lefebvre, T., Campas, M., Matta, K., Ouzia, S., Guitton, Y., Duval, G., Ploteau, S., Marchand, P., Bizec, B. L., Fréour, T., et al. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.170678 · Cited by 8
OMICs Studies and Endometriosis Biomarker Identification
Saare, M., Peters, M., Aints, A., Laisk, T., Salumets, A., & Altmäe, S. (2017) · Springer eBooks · doi:10.1007/978-3-319-59856-7_12 · Cited by 8
Correlation between lipid metabolism and endometriosis: a meta-analysis
Yang, X., Xue, X., Zhu, Y., & Zhang, Z. (2025) · Gynecological Endocrinology · doi:10.1080/09513590.2025.2500459 · Cited by 7
[Research progress on biomarkers for endometriosis based on lipidomics].
Lin, C., Chen, Z., Wang, C., & Xi, Y. (2020) · PubMed Central · doi:10.3785/j.issn.1008-9292.2020.12.14 · Cited by 7
Current Role of Modern Chromatography with Mass Spectrometry and Nuclear Magnetic Resonance Spectroscopy in the Investigation of Biomarkers of Endometriosis
Kartsova, L. A., Бессонова, Е. А., Deev, V., & Алексеевна, К. Е. (2023) · Critical Reviews in Analytical Chemistry · doi:10.1080/10408347.2022.2156770 · Cited by 7
Antibody Arrays Identified Cycle-Dependent Plasma Biomarker Candidates of Peritoneal Endometriosis
Pušić, M. N., Klančič, T., Knific, T., Vogler, A., Schmidt, R., Schröder, C., & Rižner, T. L. (2022) · Journal of Personalized Medicine · doi:10.3390/jpm12060852 · Cited by 7
Self-citation
The strategic role of lipidomics in biomarker identification and diagnosis of gynecological diseases
Hou, M., Chu, X., Wang, S., Zhang, Q., Ma, M., & Ma, J. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1546512 · Cited by 6
Dysregulation in Sphingolipid Signaling Pathways is Associated With Symptoms and Functional Connectivity of Pain Processing Brain Regions in Provoked Vestibulodynia
Labus, J. S., Mayer, E. A., Tillisch, K., Aagaard, K. M., Stains, J., Broniowska, K., Remortel, C. V., Tun, G., & Rapkin, A. J. (2021) · Journal of Pain · doi:10.1016/j.jpain.2021.04.017 · Cited by 6
Metabolic reprogramming in endometriosis: mechanisms and therapeutic prospects
Guo, C., Na, X., Guo, Z., Jiao, J., Yang, M., Liang, J., Dai, W., Na, Z., Jiang, Z., Li, Y., et al. (2026) · Journal of Advanced Research · doi:10.1016/j.jare.2026.04.069 · Cited by 6
Dual mass spectrometry as a tool to improve annotation and quantification in targeted plasma lipidomics
Gao, L., Cazenave‐Gassiot, A., Burla, B., Wenk, M. R., & Torta, F. T. (2020) · Metabolomics · doi:10.1007/s11306-020-01677-z · Cited by 5
Comparative analysis of the molecular composition of ectopic and eutopic endometrium evaluated by mass spectrometry and immunohistochemistry in endometriosis
Borisova, A. V., Kozachenko, K. A. V., Starodubtseva, N. L., Коган, Е. А., Chagovets, V. V., Salimova, D., Kononikhin, A. S., Евгеньевич, Ф. В., & Adamyan, L. V. (2017) · Russian Journal of Human Reproduction · doi:10.17116/repro201723154-60 · Cited by 4

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
ORCID: Scherb, H.
Möller, G.
Prehn, C.
Rižner, T. Lanišnik
Adamski, J.
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
DOI: 10.1093/humrep/des152
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: green
repozitorij.uni-lj.si
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

Discovery of phosphatidylcholines and sphingomyelins as biomarkers for ovarian endometriosis

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks