Genome-Wide Association Study Link Novel Loci to Endometriosis
Open accessAbstract
Endometriosis is a common gynecological condition with complex etiology defined by the presence of endometrial glands and stroma outside the womb. Endometriosis is a common cause of both cyclic and chronic pelvic pain, reduced fertility, and reduced quality-of-life. Diagnosis and treatment of endometriosis is, on average, delayed by 7-10 years from the onset of symptoms. Absence of a timely and non-invasive diagnostic tool is presently the greatest barrier to the identification and treatment of endometriosis. Twin and family studies have documented an increased relative risk in families. To identify genetic factors that contribute to endometriosis we conducted a two-stage genome-wide association study (GWAS) of a European cohort including 2,019 surgically confirmed endometriosis cases and 14,471 controls. Three of the SNPs we identify associated at P<5×10(-8) in our combined analysis belong to two loci: LINC00339-WNT4 on 1p36.12 (rs2235529; P = 8.65×10(-9), OR = 1.29, CI = 1.18-1.40) and RND3-RBM43 on 2q23.3 (rs1519761; P = 4.70×10(-8), OR = 1.20, Cl = 1.13-1.29, and rs6757804; P = 4.05×10(-8), OR = 1.20, Cl = 1.13-1.29). Using an adjusted Bonferoni significance threshold of 4.51×10(-7) we identify two additional loci in our meta-analysis that associate with endometriosis:, RNF144B-ID4 on 6p22.3 (rs6907340; P = 2.19×10(-7), OR = 1.20, Cl = 1.12-1.28), and HNRNPA3P1-LOC100130539 on 10q11.21 (rs10508881; P = 4.08×10(-7), OR = 1.19, Cl = 1.11-1.27). Consistent with previously suggested associations to WNT4 our study implicate a 150 kb region around WNT4 that also include LINC00339 and CDC42. A univariate analysis of documented infertility, age at menarche, and family history did not show allelic association with these SNP markers. Clinical data from patients in our study reveal an average delay in diagnosis of 8.4 years and confirm a strong correlation between endometriosis severity and infertility (n = 1182, P<0.001, OR = 2.18). This GWAS of endometriosis was conducted with high diagnostic certainty in cases, and with stringent handling of population substructure. Our findings broaden the understanding of the genetic factors that play a role in endometriosis.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
SNPs LINC00339-WNT4 at locus 1p36.12 (rs2235529) and RND3-RBM43 at locus 2q23.3 (rs1519761 and rs6757804) are associated with endometriosis.
“Three of the single nucleotide polymorphisms (SNPs) associated with the disease have been identified: LINC00339-WNT4 at locus 1p36.12 (rs2235529) and RND3-RBM43 at locus 2q23.3 (rs1519761 and rs6757804).”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [188]
Meta-analysis identified two additional loci associated with endometriosis: RNF144B-ID4 at 6p22.3 (rs6907340) and HNRNPA3P1-LOC100130539 at 10q11.21 (rs10508881).
“The meta-analysis identified two additional loci that were associated with endometriosis: RNF144B-ID4 at 6p22.3 (rs6907340) and HNRNPA3P1-LOC100130539at 10q11.21 (rs10508881).”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [188]
GWA studies have identified 11 independent SNPs for endometriosis.
“Genome-wide association (GWA) studies have identified 11 independent single-nucleotide polymorphisms (SNPs) for endometriosis.”
From Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism (2017) · cites this paper as [6]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
PLINK: a tool set for whole-genome association and population-based linkage analyses.
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., et al. (2007) · The American Journal of Human Genetics · doi:10.1086/519795 · Cited by 34,089 · see citing works
Principal components analysis corrects for stratification in genome-wide association studies
Price, A. L., Patterson, N. J., Plenge, R. M., Weinblatt, M. E., Shadick, N. A., & Reich, D. (2006) · Nature Genetics · doi:10.1038/ng1847 · Cited by 10,248 · see citing works
Fast model-based estimation of ancestry in unrelated individuals
Alexander, D. H., Novembre, J., & Lange, K. (2009) · Genome Research · doi:10.1101/gr.094052.109 · Cited by 9,898 · see citing works
A note on a general definition of the coefficient of determination
NAGELKERKE, N. J. D. (1991) · Biometrika · doi:10.1093/biomet/78.3.691 · Cited by 5,927 · see citing works
Howie, B. N., Donnelly, P., & Marchini, J. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000529 · Cited by 3,928 · see citing works
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166 · 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
Genetics in geographically structured populations: defining, estimating and interpreting FST
Holsinger, K. E., & Weir, B. S. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2611 · Cited by 1,422 · see citing works
Ballard, K., Lowton, K., & Wright, J. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.04.054 · Cited by 628 · see citing works
Arruda, M. S. (2003) · Human Reproduction · doi:10.1093/humrep/deg136 · Cited by 373 · see citing works
Genetic influences on endometriosis in an Australian twin sample
Treloar, S. A., O’Connor, D. T., O’Connor, V. M., & Martin, N. G. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00540-8 · Cited by 353 · see citing works
Genome-wide association meta-analysis identifies new endometriosis risk loci
Nyholt, D. R., Low, S.-K., Anderson, C. A., Painter, J. N., Uno, S., Morris, A. P., MacGregor, S., Gordon, S. D., Henders, A. K., Martin, N. G., et al. (2012) · Nature Genetics · doi:10.1038/ng.2445 · Cited by 315 · see citing works
Genome-wide association study identifies a locus at 7p15.2 associated with endometriosis
Painter, J. N., Anderson, C. A., Nyholt, D. R., Macgregor, S., Lin, J., Lee, S. H., Lambert, A., Zhao, Z. Z., Roseman, F., Guo, Q., et al. (2011) · Nature Genetics · doi:10.1038/ng.731 · Cited by 308 · 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
Nelson, M. R., Bryc, K., King, K. S., Indap, A., Boyko, A. R., Novembre, J., Briley, L. P., Maruyama, Y., Waterworth, D. M., Waeber, G., et al. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.08.005 · Cited by 293 · see citing works
Franco, H. L., Dai, D., Lee, K. Y., Rubel, C. A., Roop, D. R., Boerboom, D., Jeong, J., Lydon, J. P., Bagchi, I. C., Bagchi, M. K., et al. (2010) · The FASEB Journal · doi:10.1096/fj.10-175349 · Cited by 273 · see citing works
Uno, S., Zembutsu, H., Hirasawa, A., Takahashi, A., Kubo, M., Akahane, T., Aoki, D., Kamatani, N., Hirata, K., & Nakamura, Y. (2010) · Nature Genetics · doi:10.1038/ng.612 · Cited by 259 · see citing works
Genetic factors contribute to the risk of developing endometriosis
Stefansson, H., Geirsson, R. T., Steinthorsdottir, V., Jonsson, H., Manolescu, A., Kong, A., Ingadottir, G., Gulcher, J., & Stefansson, K. (2002) · Human Reproduction · doi:10.1093/humrep/17.3.555 · Cited by 228 · see citing works
The search for genes contributing to endometriosis risk
Montgomery, G. W., Nyholt, D. R., Zhao, Z. Z., Treloar, S. A., Painter, J. N., Missmer, S. A., Kennedy, S. H., & Zondervan, K. T. (2008) · Human Reproduction Update · doi:10.1093/humupd/dmn016 · Cited by 211 · see citing works
Treloar, S. A., Wicks, J., Nyholt, D. R., Montgomery, G. W., Bahlo, M., Smith, V. E., Dawson, G., Mackay, I., Weeks, D. E., Bennett, S. T., et al. (2005) · The American Journal of Human Genetics · doi:10.1086/432960 · Cited by 195 · see citing works
Endometriosis in monozygotic twins
Hadfield, R. M., Mardon, H. J., Barlow, D. H., & Kennedy, S. H. (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)00359-2 · Cited by 166 · see citing works
Signorile, P. G., Baldi, F., Bussani, R., D'Armiento, M., De Falco, M., & Baldi, A. (2009) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-28-49 · Cited by 118 · see citing works
Endometriosis in monozygotic twins
Moen, M. H. (1994) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349409013396 · Cited by 114 · see citing works
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 102 · see citing works
A polymorphism in a let‐7 microRNA binding site of KRAS in women with endometriosis
Grechukhina, O., Petracco, R., Popkhadze, S., Massasa, E., Paranjape, T., Chan, E., Flores, I., Weidhaas, J. B., & Taylor, H. S. (2012) · EMBO Molecular Medicine · doi:10.1002/emmm.201100200 · Cited by 96 · see citing works
Insights into assessing the genetics of endometriosis
Rahmioglu, N., Missmer, S. A., Montgomery, G. W., & Zondervan, K. T. (2012) · Current Obstetrics and Gynecology Reports · doi:10.1007/s13669-012-0016-5 · Cited by 71 · see citing works
Genetics and Genomics of Endometriosis
Hansen, K. A., & Eyster, K. M. (2010) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181db7ca1 · Cited by 63 · see citing works
Hu, W.-P., Tay, S. K., & Zhao, Y. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1594 · Cited by 57 · see citing works
Goteri, G., Ciavattini, A., Lucarini, G., Montik, N., Filosa, A., Stramazzotti, D., Biagini, G., & Tranquilli, A. L. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.01.031 · Cited by 21 · see citing works
Luong, H. T., Nyholt, D. R., Painter, J. N., Chapman, B. M., Kennedy, S., Treloar, S. A., Zondervan, K. T., & Montgomery, G. W. (2012) · Human Reproduction · doi:10.1093/humrep/des329 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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 · see citing works
Smolarz, B., Szyłło, K., & Romanowicz, H. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910554 · Cited by 560 · see citing works
Theories on the pathogenesis of endometriosis
Sourial, S., Tempest, N., & Hapangama, D. K. (2014) · International Journal of Reproductive Medicine · doi:10.1155/2014/179515 · Cited by 418 · see citing works
Suda, K., Nakaoka, H., Yoshihara, K., Ishiguro, T., Tamura, R., Mori, Y., Yamawaki, K., Adachi, S., Takahashi, T., Kase, H., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.037 · Cited by 414 · see citing works
Genetic Associations with Gestational Duration and Spontaneous Preterm Birth
Zhang, G., Feenstra, B., Bačelis, J., Liu, X., Muglia, L. M., Juodakis, J., Miller, D. E., Litterman, N. K., Jiang, P., Russell, L. E., et al. (2017) · New England Journal of Medicine · doi:10.1056/nejmoa1612665 · Cited by 376 · see citing works
Sapkota, Y., Steinthorsdottir, V., Morris, A. P., Fassbender, A., Rahmioglu, N., De Vivo, I., Buring, J. E., Zhang, F., Edwards, T. L., Jones, S., et al. (2017) · Nature Communications · doi:10.1038/ncomms15539 · Cited by 344 · see citing works
Endometriosis-associated infertility: From pathophysiology to tailored treatment
Bonavina, G., & Taylor, H. S. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1020827 · Cited by 359 · see citing works
Rahmioglu, N., Nyholt, D. R., Morris, A. P., Missmer, S. A., Montgomery, G. W., & Zondervan, K. T. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu015 · Cited by 238 · see citing works
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 · see citing works
Saha, R., Pettersson, H. J., Svedberg, P., Olovsson, M., Bergqvist, A., Marions, L., Tornvall, P., & Kuja-Halkola, R. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.06.035 · Cited by 211 · see citing works
Diagnosis of endometriosis in the 21st century
Kiesel, L., & Sourouni, M. (2019) · Climacteric · doi:10.1080/13697137.2019.1578743 · Cited by 192 · see citing works
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 188 · see citing works
Endometriosis: A Disease That Remains Enigmatic
Acién, P., & Velasco, I. (2013) · ISRN Obstetrics and Gynecology · doi:10.1155/2013/242149 · Cited by 182 · see citing works
Recent insights on the genetics and epigenetics of endometriosis
Borghese, B., Zondervan, K. T., Abrão, M. S., Chapron, C., & Vaiman, D. (2016) · Clinical Genetics · doi:10.1111/cge.12897 · Cited by 162 · see citing works
Gallagher, C. S., Mäkinen, N., Harris, H. R., Rahmioğlu, N., Uimari, O., Cook, J. P., Shigesi, N., Ferreira, T. C., Velez-Edwards, D. R., Edwards, T. L., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12536-4 · Cited by 169 · see citing works
Molecular Basis of Endometriosis and Endometrial Cancer: Current Knowledge and Future Perspectives
Terzić, M., Aimagambetova, G. N., Kunz, J., Bapayeva, G., Aitbayeva, B., Terzic, S., & Laganà, A. S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179274 · Cited by 111 · see citing works
Dawson, A., Llauradó Fernandez, M., Anglesio, M., Yong, P. J., & Carey, M. S. (2018) · ecancermedicalscience · doi:10.3332/ecancer.2018.803 · Cited by 106 · see citing works
Uimari, O., Rahmioğlu, N., Nyholt, D. R., Vincent, K., Missmer, S. A., Becker, C. M., Morris, A. P., Montgomery, G. W., & Zondervan, K. T. (2017) · Human Reproduction · doi:10.1093/humrep/dex024 · Cited by 107 · see citing works
Biofilms on Hospital Shower Hoses: Characterization and Implications for Nosocomial Infections
Soto-Girón, M. J., Rodriguez‐R, L. M., Luo, C., Elk, M., Ryu, H., Hoelle, J. M., Domingo, J. W. S., & Konstantinidis, K. T. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.03529-15 · Cited by 103 · see citing works
Chen, X., Zhu, D., Yang, M. G., Hu, W., Duan, Y.-Y., Lü, B.-J., Rong, Y., Dong, S., Hao, R.-H., Chen, J., et al. (2018) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2018.03.001 · Cited by 94 · see citing works
Genetic, Epigenetic, and Steroidogenic Modulation Mechanisms in Endometriosis
Zubrzycka, A., Zubrzycki, M., Perdas, E., & Zubrzycka, M. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9051309 · Cited by 97 · see citing works
Wang, X., Chen, T., Zhang, Y., Zhang, N., Li, C., Li, Y., Liu, Y., Zhang, H., Zhao, W., Chen, B., et al. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28007 · Cited by 86 · see citing works
Beyond Endometriosis Genome-Wide Association Study: From Genomics to Phenomics to the Patient
Rahmioglu, N., Morris, A., Nyholt, D., Montgomery, G., Becker, C., Missmer, S., & Zondervan, K. (2016) · Seminars in Reproductive Medicine · doi:10.1055/s-0036-1585408 · Cited by 84 · see citing works
Cardiomyopathy and Preeclampsia
Gammill, H. S., Chettier, R., Brewer, A. N., Roberts, J. M., Shree, R. S., Tsigas, E. Z., & Ward, K. J. (2018) · Circulation · doi:10.1161/circulationaha.117.031527 · Cited by 84 · see citing works
Self-citationPathogenesis of Endometriosis and Endometriosis-Associated Cancers
Adilbayeva, A., & Kunz, J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25147624 · Cited by 88 · see citing works
Association between endometriosis and the interleukin 1A (IL1A) locus
Sapkota, Y., Low, S., Attia, J., Gordon, S. D., Henders, A. K., Holliday, E. G., MacGregor, S., Martin, N. G., McEvoy, M., Morris, A. P., et al. (2014) · Human Reproduction · doi:10.1093/humrep/deu267 · Cited by 75 · see citing works
Rahmioğlu, N., Montgomery, G. W., & Zondervan, K. T. (2015) · Women s Health · doi:10.2217/whe.15.41 · Cited by 73 · see citing works
Sources of Individual Differences in Pain
Mogil, J. S. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-092820-105941 · Cited by 73 · see citing works
Ruth, K. S., Beaumont, R. N., Tyrrell, J., Jones, S. E., Tuke, M. A., Yaghootkar, H., Wood, A. R., Freathy, R. M., Weedon, M. N., Frayling, T. M., et al. (2016) · Human Reproduction · doi:10.1093/humrep/dev318 · Cited by 70 · see citing works
New concepts on the etiology of endometriosis
Cousins, F. L., McKinnon, B. D., Mortlock, S., Fitzgerald, H. C., Zhang, C., Montgomery, G. W., & Gargett, C. E. (2023) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.15549 · Cited by 82 · see citing works
Identifying the Biological Basis of GWAS Hits for Endometriosis1
Fung, J. N., Rogers, P. A. W., & Montgomery, G. W. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.114.126458 · Cited by 69 · see citing works
Endometriosis: A Review of Clinical Diagnosis, Treatment, and Pathogenesis
Chauhan, S., More, A., Chauhan, V. V. S., & Kathane, A. (2022) · Cureus · doi:10.7759/cureus.28864 · Cited by 78 · see citing works
Pathophysiological Functions of Rnd 3/ RhoE
Jie, W., Andrade, K. C., Lin, X., Yang, X., Yue, X., & Chang, J. (2015) · Comprehensive physiology · doi:10.1002/cphy.c150018 · Cited by 65 · see citing works
Monsivais, D., Dyson, M. T., Yin, P., Navarro, A., Coon, J. S., Pavone, M. E., & Bulun, S. E. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.01.012 · Cited by 62 · see citing works
Systems genetics view of endometriosis: a common complex disorder
Baranov, V. S., Ivaschenko, T. E., Liehr, T., & Yarmolinskaya, M. I. (2015) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.11.036 · Cited by 62 · see citing works
Jones, A. V., Hockley, J. R. F., Hyde, C. L., Gorman, D. N., Sredic-Rhodes, A., Bilsland, J., McMurray, G., Furlotte, N. A., Hu, Y., Hinds, D. A., et al. (2016) · Pain · doi:10.1097/j.pain.0000000000000678 · Cited by 65 · see citing works
Whole-genome sequencing identifies potential candidate genes for reproductive traits in pigs
Li, X., Ye, J., Han, X., Qiao, R., Li, X., Lv, G., & Wang, K. (2019) · Genomics · doi:10.1016/j.ygeno.2019.01.014 · Cited by 60 · see citing works
Endometriosis risk alleles at 1p36.12 act through inverse regulation ofCDC42andLINC00339
Powell, J. E., Fung, J. N., Shakhbazov, K., Sapkota, Y., Cloonan, N., Hemani, G., Hillman, K. M., Kaufmann, S., Luong, H. T., Bowdler, L. M., et al. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw320 · Cited by 57 · see citing works
IL-33 activates group 2 innate lymphoid cell expansion and modulates endometriosis
Miller, J. E., Lingegowda, H., Symons, L. K., Bougie, O., Young, S. L., Lessey, B. A., Koti, M., & Tayade, C. (2021) · JCI Insight · doi:10.1172/jci.insight.149699 · Cited by 55 · see citing works
Candidate genes for age at menarche are associated with endometriosis
Ponomarenko, I., Reshetnikov, E., Polonikov, A., Verzilina, I., Sorokina, I., Elgaeva, E. E., Tsepilov, Y. A., Yermachenko, A., Dvornyk, V., & Churnosov, M. (2020) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2020.04.016 · Cited by 49 · see citing works
Should genetics now be considered the pre-eminent etiologic factor in endometriosis?
Montgomery, G. W., Mortlock, S., & Giudice, L. C. (2020) · Journal of Minimally Invasive Gynecology · doi:10.1016/j.jmig.2019.10.020 · Cited by 49 · see citing works
Common variants upstream of KDR encoding VEGFR2 and in TTC39B associate with endometriosis
Steinthorsdottir, V., Thorleifsson, G., Aradottir, K., Feenstra, B., Sigurdsson, A., Stefansdottir, L., Kristinsdottir, A. M., Zink, F., Halldorsson, G. H., Munk Nielsen, N., et al. (2016) · Nature Communications · doi:10.1038/ncomms12350 · Cited by 48 · see citing works
Albertsen, H., & Ward, K. J. (2016) · Reproductive Sciences · doi:10.1177/1933719116660847 · Cited by 45 · see citing works
Self-citationThe future for genetic studies in reproduction
Montgomery, G. W., Zondervan, K. T., & Nyholt, D. R. (2013) · Molecular Human Reproduction · doi:10.1093/molehr/gat058 · Cited by 47 · see citing works
Defining the genetic profile of endometriosis (Review)
Vassilopoulou, L., Matalliotakis, M., Zervou, M. I., Matalliotaki, C., Krithinakis, K., Matalliotakis, I., Spandidos, D. A., & Goulielmos, G. N. (2019) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2019.7346 · Cited by 49 · see citing works
Nakaoka, H., Gurumurthy, A., Hayano, T., Ahmadloo, S., Omer, W. H., Yoshihara, K., Yamamoto, A., Kurose, K., Enomoto, T., Akira, S., et al. (2016) · PLOS Genetics · doi:10.1371/journal.pgen.1005893 · Cited by 46 · see citing works
Association of WNT4 polymorphisms with endometriosis in infertile patients
Mafra, F., Catto, M., Bianco, B. A. V., Barbosa, C. P., & Christofolini, D. M. (2015) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-015-0523-1 · Cited by 45 · see citing works
Rare coding variants pinpoint genes that control human hematological traits
Mousas, A., Ntritsos, G., Chen, M., Song, C., Huffman, J. E., Tzoulaki, I., Elliott, P., Psaty, B. M., Auer, P. L., Johnson, A. D., et al. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006925 · Cited by 43 · see citing works
Rahmioğlu, N., Drong, A., Lockstone, H. E., Tapmeier, T. T., Hellner, K., Saare, M., Laisk, T., Dew, C., Tough, E., Nicholson, G., et al. (2017) · Epigenetics · doi:10.1080/15592294.2017.1367475 · Cited by 44 · see citing works
Independent Replication and Meta-Analysis for Endometriosis Risk Loci
Sapkota, Y., Fassbender, A., Bowdler, L., Fung, J. N., Peterse, D., O, D., Montgomery, G. W., Nyholt, D. R., & D'Hooghe, T. M. (2015) · Twin Research and Human Genetics · doi:10.1017/thg.2015.61 · Cited by 43 · see citing works
Endometrial vezatin and its association with endometriosis risk
Holdsworth-Carson, S. J., Fung, J. N., Luong, H. T. T., Sapkota, Y., Bowdler, L. M., Wallace, L., Teh, W. T., Powell, J. E., Girling, J. E., Healey, M., et al. (2016) · Human Reproduction · doi:10.1093/humrep/dew047 · Cited by 41 · see citing works
Genetics of endometriosis: state of the art on genetic risk factors for endometriosis
Fung, J. N., & Montgomery, G. W. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.01.012 · Cited by 41 · see citing works
New Insights into Genetics of Endometriosis—A Comprehensive Literature Review
Chiorean, D. M., Mitranovici, M.-I., Toru, H. S., Cotoi, T. C., Tomuț, A. N., Turdean, S. G., & Cotoi, O. S. (2023) · Diagnostics · doi:10.3390/diagnostics13132265 · Cited by 41 · see citing works
Borghese, B., Santulli, P., Marcellin, L., & Chapron, C. (2018) · Gynécologie Obstétrique Fertilité & Sénologie · doi:10.1016/j.gofs.2018.02.017 · Cited by 42 · see citing works
Genomics of Endometriosis: From Genome Wide Association Studies to Exome Sequencing
Lalami, I., Abo, C., Borghese, B., Chapron, C., & Vaiman, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147297 · Cited by 44 · see citing works
Pagliardini, L., Gentilini, D., Sanchez, A. M., Candiani, M., Viganò, P., & Di Blasio, A. M. (2015) · Human Reproduction · doi:10.1093/humrep/dev022 · Cited by 37 · see citing works
Borghese, B., Tost, J., de Surville, M., Busato, F., Letourneur, F., Mondon, F., Vaiman, D., & Chapron, C. (2015) · BioMed Research International · doi:10.1155/2015/461024 · Cited by 38 · see citing works
Systematic review of genome-wide association studies on susceptibility to endometriosis
Cardoso, J. V., Perini, J. A., Machado, D. E., Pinto, R., & Medeiros, R. (2020) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2020.10.017 · Cited by 36 · see citing works
Butler, M. G., McGuire, A., & Manzardo, A. M. (2015) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-014-0411-0 · Cited by 35 · see citing works
Feng, H., Liu, J., Qiu, Y., Liu, Y., Saiyin, H., Liang, X., Zheng, F., Wang, Y., Jiang, D., Wang, Y., et al. (2020) · Oncogene · doi:10.1038/s41388-020-1380-7 · Cited by 35 · see citing works
Zhao, H., & Chen, Z. (2013) · Molecular Human Reproduction · doi:10.1093/molehr/gat040 · Cited by 33 · see citing works
Bao, C., Wang, H., & Fang, H. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.758440 · Cited by 35 · see citing works
Diagnostic Potential of Cytokine Biomarkers in Endometriosis: Challenges and Insights
Krygere, L., Jukna, P., Jarienė, K., & Drejerienė, E. (2024) · Biomedicines · doi:10.3390/biomedicines12122867 · Cited by 33 · see citing works
Genomic regions underlying susceptibility to bovine tuberculosis in Holstein-Friesian cattle
Raphaka, K., Matika, O., Sánchez-Molano, E., Mrode, R., Coffey, M. P., Riggio, V., Glass, E. J., Woolliams, J. A., Bishop, S. C., & Banos, G. (2017) · BMC Genetics · doi:10.1186/s12863-017-0493-7 · Cited by 32 · see citing works
The role of IL‑16 gene polymorphisms in endometriosis
Matalliotakis, M., Zervou, M. I., Eliopoulos, E., Matalliotaki, C., Rahmioğlu, N., Kalogiannidis, I. A., Zondervan, K. T., Spandidos, D. A., Matalliotakis, I., & Goulielmos, G. N. (2018) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2018.3368 · Cited by 30 · see citing works
Wang, Z., Zhang, J.-W., Zhang, Y., Zhang, S., Hu, Q., & Liang, H. (2018) · Urolithiasis · doi:10.1007/s00240-018-1065-7 · Cited by 30 · see citing works
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 · see citing works
Sobalska-Kwapis, M., Smolarz, B., Słomka, M., Szaflik, T., Kępka, E., Kulig, B., Siewierska-Górska, A., Polak, G., Romanowicz, H., Strapagiel, D., et al. (2017) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2017.08.037 · Cited by 29 · see citing works
Sapkota, Y., Vivo, I. D., Steinthórsdóttir, V., Fassbender, A., Bowdler, L. M., Buring, J. E., Edwards, T. L., Jones, S. F., Dorien, O., Peterse, D., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-10440-9 · Cited by 30 · see citing works
Epithelial Cells of Deep Infiltrating Endometriosis Harbor Mutations in Cancer Driver Genes
Koppolu, A. A., Maksym, R., Paskal, W., Machnicki, M. M., Rak, B., Pępek, M., Garbicz, F., Pełka, K., Kuśmierczyk, Z., Jacko, J., et al. (2021) · Cells · doi:10.3390/cells10040749 · Cited by 27 · see citing works
Fine mapping of variants associated with endometriosis in the WNT4 region on chromosome 1p36.
Luong, H. T., Painter, J. N., Shakhbazov, K., Chapman, B. M., Henders, A. K., Powell, J. E., Nyholt, D. R., & Montgomery, G. W. (2013) · Europe PMC (PubMed Central) · Cited by 24 · see citing works
Evaluation of miR‑135a/b expression in endometriosis lesions
Petracco, R. G., Dias, A., Taylor, H. S., Petracco, �., Badalotti, M., Michelon, J., Marinowic, D. R., Hentschke, M. R., de Azevedo, P., Zanirati, G., et al. (2019) · Biomedical Reports · doi:10.3892/br.2019.1237 · Cited by 25 · see citing works
Zhao, L., Gu, C., Huang, K., Fan, W., Li, J., Ye, M., Han, W., & Meng, Y. (2016) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2016.06.003 · Cited by 24 · see citing works
Kim, H., Lee, H., Kazmi, S. Z., Hann, H. J., Kang, T., Cha, J., Choi, S.-B., Swan, H., Kim, H. J., Lee, Y.-S., et al. (2021) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.16769 · Cited by 23 · see citing works
Association of CDKN2B-AS and WNT4 genetic polymorphisms in Korean patients with endometriosis
Lee, G. H., Choi, Y. M., Hong, M. A., Yoon, S. H., Kim, J., Hwang, K., & Chae, S. J. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.07.1237 · Cited by 23 · see citing works
Analysis of WNT4 polymorphism in Chinese Han women with endometriosis
Wu, Z., Yuan, M., Li, Y., Fu, F., Ma, W., Li, H., Wang, W., & Wang, S. (2015) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2014.12.010 · Cited by 22 · see citing works
Smolarz, B., Szyłło, K., & Romanowicz, H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218235 · Cited by 23 · see citing works
Geysenbergh, B., Dancet, E. A. F., & D'Hooghe, T. (2017) · Gynecologic and Obstetric Investigation · doi:10.1159/000452098 · Cited by 24 · see citing works
Kobayashi, H., Uekuri, C., & Shigetomi, H. (2013) · Gynecological Endocrinology · doi:10.3109/09513590.2013.831832 · Cited by 21 · see citing works
Osiński, M., Mostowska, A., Wirstlein, P., Wender-Ożegowska, E., Jagodziński, P. P., & Szczepańska, M. (2018) · Ginekologia Polska · doi:10.5603/gp.a2018.0052 · Cited by 19 · see citing works
WNT4 Balances Development vs Disease in Gynecologic Tissues and Women’s Health
Pitzer, L. M., Moroney, M. R., Nokoff, N., & Sikora, M. J. (2021) · Endocrinology · doi:10.1210/endocr/bqab093 · Cited by 22 · see citing works
Li, Y., Hao, N., Wang, Y., & Kang, S. (2016) · Reproductive Sciences · doi:10.1177/1933719116650753 · Cited by 20 · see citing works
Copy number variation analysis reveals additional variants contributing to endometriosis development
Mafra, F., Mazzotti, D. R., Pellegrino, R., Bianco, B. A. V., Barbosa, C. P., Hakonarson, H. H., & Christofolini, D. M. (2016) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-016-0822-1 · Cited by 19 · see citing works
Luo, Y., Liu, L., Li, X., & Shi, Y. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110508 · Cited by 20 · see citing works
Mascarenhas, R., Pietrzak, M., Smith, R. M., Webb, A., Wang, D., Papp, A. C., Pinsonneault, J. K., Seweryn, M. T., Rempała, G. A., & Sadée, W. (2015) · PLoS ONE · doi:10.1371/journal.pone.0136798 · Cited by 18 · see citing works
Wang, W., Li, Y., Li, S., Wu, Z., Yuan, M., Wang, T., & Wang, S. (2016) · Reproductive Sciences · doi:10.1177/1933719116657191 · Cited by 16 · see citing works
Endometriosis Is Associated with Rare Copy Number Variants
Chettier, R., Ward, K. J., & Albertsen, H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103968 · Cited by 16 · see citing works
Self-citationChou, Y., Chen, M.-J., Chen, P.-H., Chang, C., Yu, M., Chen, Y., Tsai, E., Tsai, S., Kuo, W.-S., & Tzeng, C. (2021) · Scientific Reports · doi:10.1038/s41598-020-79515-4 · Cited by 14 · see citing works
Imprinting genes associated with endometriosis
Kobayashi, H. (2014) · Europe PMC (PubMed Central) · doi:10.17877/de290r-176 · Cited by 14 · see citing works
The long road of drug development for endometriosis – Pains, gains, and hopes
Liao, Z., Monsivais, D., & Matzuk, M. M. (2024) · Journal of Controlled Release · doi:10.1016/j.jconrel.2024.10.036 · Cited by 15 · see citing works
Dissecting the shared genetic architecture between endometriosis and polycystic ovary syndrome
Tan, H.-J., Long, P., & Xiao, H. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1359236 · Cited by 15 · see citing works
Molecular-genetic determinants of the development of endometriosis
Ponomarenko, I., Polonikov, A., Николаевна, В. И., & Churnosov, M. I. (2019) · Voprosy ginekologii akušerstva i perinatologii · doi:10.20953/1726-1678-2019-1-82-86 · Cited by 12 · see citing works
Kang, S. W. (2013) · Apple Academic Press eBooks · doi:10.1201/b14910-12 · Cited by 23 · see citing works
Kliber, M., Kulczyńska-Figurny, K., Jagodziński, P. P., & Pławski, A. (2025) · Journal of Applied Genetics · doi:10.1007/s13353-025-01021-y · Cited by 10 · see citing works
Molecular Mechanisms of Endometriosis Revealed Using Omics Data
Cho, S. B. (2023) · Biomedicines · doi:10.3390/biomedicines11082210 · Cited by 10 · see citing works
Butler, M. G., Rafi, S. K., McGuire, A., & Manzardo, A. M. (2015) · Gene · doi:10.1016/j.gene.2015.08.057 · Cited by 10 · see citing works
Microvesicles released from ectopic endometrial foci as a potential biomarker of endometriosis
Kajdos, M., Szymański, J., Jerczyńska, H., Stetkiewicz, T., & Wilczyński, J. R. (2022) · Ginekologia Polska · doi:10.5603/gp.a2022.0096 · Cited by 9 · see citing works
Whole-exome sequencing reveals candidate high-risk susceptibility genes for endometriosis
Nousiainen, S., Kuismin, O., Reinikka, S., Manninen, R., Khamaiseh, S., Kuivalainen, M., Terho, A., Koivurova, S., Niinimäki, M. J., Salokas, K., et al. (2023) · Human Genomics · doi:10.1186/s40246-023-00538-9 · Cited by 9 · see citing works
Birt, J. A., Taylor, K. H., Davis, J., & Sharpe-Timms, K. L. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.07.007 · Cited by 9 · see citing works
Gallagher, C. S., Mäkinen, N., Harris, H. R., Uimari, O., Cook, J. P., Shigesi, N., Rahmioğlu, N., Ferreira, T. C., Velez-Edwards, D. R., Edwards, T. L., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/324905 · Cited by 9 · see citing works
- Authors
- Albertsen, H. M., Chettier, R., Farrington, P., & Ward, K.
- Corresponding author
- Ward, Kenneth
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-03-05
- Volume
- 8
- Issue
- 3
- Pages
- e58257
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3589333
- OpenAlex
- W2051994829
- Cited by
- 161
- References
- 30
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 7 · 2023: 9 · 2022: 7 · 2021: 14 · 2020: 9 · 2019: 13 · 2018: 18 · 2017: 17 · 2016: 20 · 2015: 16 · 2014: 9 · 2013: 11
- FWCI
- 22.54
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and fungal interactions
- Keywords
- endometriosis, genetic susceptibility, genetic loci, single nucleotide polymorphisms, endometriosis diagnosis
- MeSH terms
- Adult, Algorithms, Alleles, Endometriosis, Female, Genotype, Humans, Software, Reproducibility of Results, Cohort Studies, Case-Control Studies, Genetic Predisposition to Disease, Polymorphism, Single Nucleotide, Principal Component Analysis, Genome-Wide Association Study, Young Adult
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
