A comprehensive analysis of germline predisposition to early-onset ovarian cancer.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
13 Jul 2024
Historique:
received: 26 02 2024
accepted: 01 07 2024
medline: 14 7 2024
pubmed: 14 7 2024
entrez: 13 7 2024
Statut: epublish

Résumé

The subset of ovarian cancer (OC) diagnosed ≤ 30yo represents a distinct subgroup exhibiting disparities from late-onset OC in many aspects, including indefinite germline cancer predisposition. We performed DNA/RNA-WES with HLA-typing, PRS assessment and survival analysis in 123 early-onset OC-patients compared to histology/stage-matched late-onset and unselected OC-patients, and population-matched controls. Only 6/123(4.9%) early-onset OC-patients carried a germline pathogenic variant (GPV) in high-penetrance OC-predisposition genes. Nevertheless, our comprehensive germline analysis of early-onset OC-patients revealed two divergent trajectories of potential germline susceptibility. Firstly, overrepresentation analysis highlighted a connection to breast cancer (BC) that was supported by the CHEK2 GPV enrichment in early-onset OC(p = 1.2 × 10

Identifiants

pubmed: 39003285
doi: 10.1038/s41598-024-66324-2
pii: 10.1038/s41598-024-66324-2
doi:

Substances chimiques

Checkpoint Kinase 2 EC 2.7.1.11

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

16183

Subventions

Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-03-00016
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-03-00016
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-03-00016
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-03-00016
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-09-00355
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : RVO-VFN 00064165
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-09-00355
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : RVO-VFN 00064165
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : RVO-VFN 00064165
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : RVO-VFN 00064165
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : RVO-VFN 00064165
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : RVO-VFN 00064165
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : RVO-VFN 00064165
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-03-00016
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-03-00016
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-03-00016
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU20-03-00016
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : SVV260631
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Univerzita Karlova v Praze
ID : COOPERATIO
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : The National Center for Medical Genomics (LM2023067)
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102
Organisme : Ministerstvo Školství, Mládeže a Tělovýchovy
ID : LX22NPO05102

Informations de copyright

© 2024. The Author(s).

Références

SEER. https://seer.cancer.gov/statfacts/html/ovary.html .
Labidi-Galy, S. I. et al. High grade serous ovarian carcinomas originate in the fallopian tube. Nat. Commun. 8, 1093. https://doi.org/10.1038/s41467-017-00962-1 (2017).
doi: 10.1038/s41467-017-00962-1 pubmed: 29061967 pmcid: 5653668
Lisio, M. A., Fu, L., Goyeneche, A., Gao, Z. H. & Telleria, C. High-grade serous ovarian cancer: Basic sciences, clinical and therapeutic standpoints. Int. J. Mol. Sci. 20, 952. https://doi.org/10.3390/ijms20040952 (2019).
doi: 10.3390/ijms20040952 pubmed: 30813239 pmcid: 6412907
Pearce, C. L. et al. Population distribution of lifetime risk of ovarian cancer in the United States. Cancer Epidemiol. Biomarkers Prev. 24, 671–676. https://doi.org/10.1158/1055-9965.EPI-14-1128 (2015).
doi: 10.1158/1055-9965.EPI-14-1128 pubmed: 25623732 pmcid: 4892114
Flaum, N., Crosbie, E. J., Edmondson, R. J., Smith, M. J. & Evans, D. G. Epithelial ovarian cancer risk: A review of the current genetic landscape. Clin. Genet. https://doi.org/10.1111/cge.13566 (2019).
doi: 10.1111/cge.13566 pubmed: 31099061 pmcid: 7017781
Lhotova, K. et al. Multigene panel germline testing of 1333 Czech patients with ovarian cancer. Cancers (Basel) 12, 956. https://doi.org/10.3390/cancers12040956 (2020).
doi: 10.3390/cancers12040956 pubmed: 32295079
Stratton, J. F. et al. The genetic epidemiology of early-onset epithelial ovarian cancer: A population-based study. Am. J. Hum. Genet. 65, 1725–1732. https://doi.org/10.1086/302671 (1999).
doi: 10.1086/302671 pubmed: 10577927 pmcid: 1288384
Flaum, N. et al. MSH2 is the very young onset ovarian cancer predisposition gene, not BRCA1. J. Med. Genet. https://doi.org/10.1136/jmg-2022-109055 (2023).
doi: 10.1136/jmg-2022-109055 pubmed: 36894311
Herold, N. et al. Pathogenic germline variants in SMARCA4 and further cancer predisposition genes in early onset ovarian cancer. Cancer Med. 12, 15256–15260. https://doi.org/10.1002/cam4.6214 (2023).
doi: 10.1002/cam4.6214 pubmed: 37345881 pmcid: 10417158
Carter, N. J. et al. Germline pathogenic variants identified in women with ovarian tumors. Gynecol. Oncol. 151, 481–488. https://doi.org/10.1016/j.ygyno.2018.09.030 (2018).
doi: 10.1016/j.ygyno.2018.09.030 pubmed: 30322717
Horackova, K., Janatova, M., Kleiblova, P., Kleibl, Z. & Soukupova, J. Early-onset ovarian cancer <30 years: What do we know about its genetic predisposition?. Int. J. Mol. Sci. 24, 17020. https://doi.org/10.3390/ijms242317020 (2023).
doi: 10.3390/ijms242317020 pubmed: 38069345 pmcid: 10707471
Bolton, K. L. et al. Common variants at 19p13 are associated with susceptibility to ovarian cancer. Nat. Genet. 42, 880–884. https://doi.org/10.1038/ng.666 (2010).
doi: 10.1038/ng.666 pubmed: 20852633 pmcid: 3125495
Dareng, E. O. et al. Polygenic risk modeling for prediction of epithelial ovarian cancer risk. Eur. J. Hum. Genet. 30, 349–362. https://doi.org/10.1038/s41431-021-00987-7 (2022).
doi: 10.1038/s41431-021-00987-7 pubmed: 35027648 pmcid: 8904525
Goode, E. L. et al. A genome-wide association study identifies susceptibility loci for ovarian cancer at 2q31 and 8q24. Nat. Genet. 42, 874–879. https://doi.org/10.1038/ng.668 (2010).
doi: 10.1038/ng.668 pubmed: 20852632 pmcid: 3020231
Jervis, S. et al. A risk prediction algorithm for ovarian cancer incorporating BRCA1, BRCA2, common alleles and other familial effects. J. Med. Genet. 52, 465–475. https://doi.org/10.1136/jmedgenet-2015-103077 (2015).
doi: 10.1136/jmedgenet-2015-103077 pubmed: 26025000
Kuchenbaecker, K. B. et al. Evaluation of polygenic risk scores for breast and ovarian cancer risk prediction in BRCA1 and BRCA2 mutation carriers. J. Natl. Cancer Inst. 109, dwj302. https://doi.org/10.1093/jnci/djw302 (2017).
doi: 10.1093/jnci/djw302
Permuth-Wey, J. et al. Identification and molecular characterization of a new ovarian cancer susceptibility locus at 17q21.31. Nat. Commun. 4, 1627. https://doi.org/10.1038/ncomms2613 (2013).
doi: 10.1038/ncomms2613 pubmed: 23535648
Pharoah, P. D. et al. GWAS meta-analysis and replication identifies three new susceptibility loci for ovarian cancer. Nat. Genet. 45, 362–370. https://doi.org/10.1038/ng.2564 (2013).
doi: 10.1038/ng.2564 pubmed: 23535730 pmcid: 3693183
Phelan, C. M. et al. Identification of 12 new susceptibility loci for different histotypes of epithelial ovarian cancer. Nat. Genet. 49, 680–691. https://doi.org/10.1038/ng.3826 (2017).
doi: 10.1038/ng.3826 pubmed: 28346442 pmcid: 5612337
Yang, X. et al. Evaluation of polygenic risk scores for ovarian cancer risk prediction in a prospective cohort study. J. Med. Genet. 55, 546 (2018).
doi: 10.1136/jmedgenet-2018-105313 pubmed: 29730597
Jia, G. et al. Evaluating the utility of polygenic risk scores in identifying high-risk individuals for eight common cancers. JNCI Cancer Spectr. 4, pkaa021. https://doi.org/10.1093/jncics/pkaa021 (2020).
doi: 10.1093/jncics/pkaa021 pubmed: 32596635 pmcid: 7306192
Kubler, K. et al. HLA-class II haplotype associations with ovarian cancer. Int. J. Cancer 119, 2980–2985. https://doi.org/10.1002/ijc.22266 (2006).
doi: 10.1002/ijc.22266 pubmed: 17016821
The NCMG research infrastructure; http://ncmg.cz .
National Marrow Donors Registry; www.allelefrequencies.net/pop6001c.asp?pop_id=3258
NCCN. Guidelines Version 2.2024: Genetic/Familial High-Risk Assessment: Breast, Ovarian, and Pancreatic, 2023).
Hovhannisyan, M. et al. Polygenic risk score (PRS) and its potential for breast cancer risk stratification. Klinicka onkologie : casopis Ceske a Slovenske onkologicke spolecnosti 36, 198–205. https://doi.org/10.48095/ccko2023198 (2023).
doi: 10.48095/ccko2023198 pubmed: 37353348
Hovhannisyan, M. et al. Population-specific validation and comparison of the performance of 77- and 313-variant polygenic risk scores for breast cancer risk prediction. Cancer https://doi.org/10.1002/cncr.35337 (2024).
doi: 10.1002/cncr.35337 pubmed: 38718029
Soukupova, J. et al. Validation of CZECANCA (CZEch CAncer paNel for Clinical Application) for targeted NGS-based analysis of hereditary cancer syndromes. PLoS One 13, e0195761. https://doi.org/10.1371/journal.pone.0195761 (2018).
doi: 10.1371/journal.pone.0195761 pubmed: 29649263 pmcid: 5896995
Horackova, K. et al. Low frequency of cancer-predisposition gene mutations in liver transplant candidates with hepatocellular carcinoma. LID - https://doi.org/10.3390/cancers15010201 (2022).
doi: 10.3390/cancers15010201
Walker, L. C. et al. Comprehensive assessment of BARD1 messenger ribonucleic acid splicing with implications for variant classification. Front. Genet. 10, 1139. https://doi.org/10.3389/fgene.2019.01139 (2019).
doi: 10.3389/fgene.2019.01139 pubmed: 31803232 pmcid: 6877745
Dobin, A. et al. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21. https://doi.org/10.1093/bioinformatics/bts635 (2013).
doi: 10.1093/bioinformatics/bts635 pubmed: 23104886
https://broadinstitute.github.io/picard/ .
Cotto, K. C. et al. Integrated analysis of genomic and transcriptomic data for the discovery of splice-associated variants in cancer. Nat. Commun. 14, 1589. https://doi.org/10.1038/s41467-023-37266-6 (2023).
doi: 10.1038/s41467-023-37266-6 pubmed: 36949070 pmcid: 10033906
Agius, P., Geiger, H. & Robine, N. SCANVIS: A tool for SCoring, ANnotating and VISualizing splice junctions. Bioinformatics 35, 4843–4845. https://doi.org/10.1093/bioinformatics/btz452 (2019).
doi: 10.1093/bioinformatics/btz452 pubmed: 31197308 pmcid: 6853764
Fadista, J., Manning, A. K., Florez, J. C. & Groop, L. The (in)famous GWAS P-value threshold revisited and updated for low-frequency variants. Eur. J. Hum. Genet. 24, 1202–1205. https://doi.org/10.1038/ejhg.2015.269 (2016).
doi: 10.1038/ejhg.2015.269 pubmed: 26733288 pmcid: 4970684
Liao, Y., Wang, J., Jaehnig, E. J., Shi, Z. & Zhang, B. WebGestalt 2019: Gene set analysis toolkit with revamped UIs and APIs. Nucleic Acids Res. 47, W199–W205. https://doi.org/10.1093/nar/gkz401 (2019).
doi: 10.1093/nar/gkz401 pubmed: 31114916 pmcid: 6602449
Wang, S. et al. SpecHLA enables full-resolution HLA typing from sequencing data. Cell Rep. Methods 3, 100589. https://doi.org/10.1016/j.crmeth.2023.100589 (2023).
doi: 10.1016/j.crmeth.2023.100589 pubmed: 37714157 pmcid: 10545945
Mavaddat, N. et al. Polygenic risk scores for prediction of breast cancer and breast cancer subtypes. Am. J. Hum. Genet. 104, 21–34. https://doi.org/10.1016/j.ajhg.2018.11.002 (2019).
doi: 10.1016/j.ajhg.2018.11.002 pubmed: 30554720
Borde, J. et al. Performance of breast cancer polygenic risk scores in 760 female CHEK2 germline mutation carriers. J. Natl. Cancer Instit. 113, 893–899. https://doi.org/10.1093/jnci/djaa203 (2021).
doi: 10.1093/jnci/djaa203
Kurman, R. J. & Shih Ie, M. The dualistic model of ovarian carcinogenesis: Revisited, revised, and expanded. Am J Pathol 186, 733–747. https://doi.org/10.1016/j.ajpath.2015.11.011 (2016).
doi: 10.1016/j.ajpath.2015.11.011 pubmed: 27012190 pmcid: 5808151
Zemankova, P. et al. A deep intronic recurrent CHEK2 variant c.1009-118_1009-87delinsC affects pre-mRNA splicing and contributes to hereditary breast cancer predisposition. Breast 75, 103721, doi:10.1016/j.breast.2024.103721 (2024).
Bonifaz, L. et al. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med 196, 1627–1638. https://doi.org/10.1084/jem.20021598 (2002).
doi: 10.1084/jem.20021598 pubmed: 12486105 pmcid: 2196060
Zelensky, A. N. & Gready, J. E. The C-type lectin-like domain superfamily. FEBS J 272, 6179–6217. https://doi.org/10.1111/j.1742-4658.2005.05031.x (2005).
doi: 10.1111/j.1742-4658.2005.05031.x pubmed: 16336259
Network, N. C. C. Genetic/Familial High-Risk Assessment: Breast, Ovarian, and Pancreatic (Version 1.2023), < https://www.nccn.org/professionals/physician_gls/pdf/genetics_bop.pdf > (2022).
Casper, A. C. et al. Risk of secondary malignancies in ovarian cancer survivors: 52,680 patients analyzed with over 40 years of follow-up. Gynecol. Oncol. 162, 454–460. https://doi.org/10.1016/j.ygyno.2021.05.034 (2021).
doi: 10.1016/j.ygyno.2021.05.034 pubmed: 34092413
Wang, J., Du, Y. & Kang, Y. Do survivors of borderline ovarian tumors have susceptibility to secondary primary malignancies? A SEER population-based study. Int. J. Gynaecol. Obstet. https://doi.org/10.1002/ijgo.15338 (2024).
doi: 10.1002/ijgo.15338 pubmed: 38993147
Kleiblova, P. et al. Parallel DNA/RNA NGS using an identical target enrichment panel in the analysis of hereditary cancer predisposition. Folia Biol (Praha) 70, 62–73. https://doi.org/10.14712/fb2024070010062 (2024).
doi: 10.14712/fb2024070010062 pubmed: 38830124
Koczkowska, M. et al. Spectrum and prevalence of pathogenic variants in ovarian cancer susceptibility genes in a group of 333 patients. Cancers (Basel) 10, 442. https://doi.org/10.3390/cancers10110442 (2018).
doi: 10.3390/cancers10110442 pubmed: 30441849
Jarhelle, E. et al. Identifying sequence variants contributing to hereditary breast and ovarian cancer in BRCA1 and BRCA2 negative breast and ovarian cancer patients. Sci. Rep. 9, 19986. https://doi.org/10.1038/s41598-019-55515-x (2019).
doi: 10.1038/s41598-019-55515-x pubmed: 31882575 pmcid: 6934654
Lawrenson, K. et al. Common variants at the CHEK2 gene locus and risk of epithelial ovarian cancer. Carcinogenesis 36, 1341–1353. https://doi.org/10.1093/carcin/bgv138 (2015).
doi: 10.1093/carcin/bgv138 pubmed: 26424751 pmcid: 4635670
Kurian, A. W. et al. Genetic Testing and results in a population-based cohort of breast cancer patients and ovarian cancer patients. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. JCO1801854, https://doi.org/10.1200/JCO.18.01854 (2019).
Stolarova, L. et al. CHEK2 Germline Variants in Cancer Predisposition: Stalemate Rather than Checkmate. Cells 9, doi:10.3390/cells9122675 (2020).
Lo, T. H. et al. Characterization of the expression and function of the C-Type lectin receptor CD302 in mice and humans reveals a role in dendritic cell migration. J. Immunol. 197, 885–898. https://doi.org/10.4049/jimmunol.1600259 (2016).
doi: 10.4049/jimmunol.1600259 pubmed: 27316686
Faddaoui, A. et al. The mannose receptor LY75 (DEC205/CD205) modulates cellular phenotype and metastatic potential of ovarian cancer cells. Oncotarget 7, 14125 (2015).
doi: 10.18632/oncotarget.7288
Mehdi, S., Bachvarova, M., Scott-Boyer, M. P., Droit, A. & Bachvarov, D. LY75 Ablation mediates mesenchymal-epithelial transition (MET) in epithelial ovarian cancer (EOC) cells associated with DNA methylation alterations and suppression of the Wnt/beta-Catenin pathway. Int. J. Mol. Sci. 21, 1848. https://doi.org/10.3390/ijms21051848 (2020).
doi: 10.3390/ijms21051848 pubmed: 32156068 pmcid: 7084525
Pagliuca, S., Gurnari, C., Rubio, M. T., Visconte, V. & Lenz, T. L. Individual HLA heterogeneity and its implications for cellular immune evasion in cancer and beyond. Front. Immunol. 13, 944872. https://doi.org/10.3389/fimmu.2022.944872 (2022).
doi: 10.3389/fimmu.2022.944872 pubmed: 36131910 pmcid: 9483928
Aureli, A. et al. Breast cancer is associated with increased HLA-DRB1*11:01 and HLA-DRB1*10:01 allele frequency in a population of patients from central Italy. Immunol. Invest. 49, 489–497. https://doi.org/10.1080/08820139.2020.1737539 (2020).
doi: 10.1080/08820139.2020.1737539 pubmed: 32183601
Tsai, S. C., Sheen, M. C. & Chen, B. H. Association between HLA-DQA1, HLA-DQB1 and oral cancer. Kaohsiung J. Med. Sci. 27, 441–445. https://doi.org/10.1016/j.kjms.2011.06.003 (2011).
doi: 10.1016/j.kjms.2011.06.003 pubmed: 21943816
Chen, P. C., Tsai, E. M., Er, T. K., Chang, S. J. & Chen, B. H. HLA-DQA1 and -DQB1 allele typing in southern Taiwanese women with breast cancer. Clin. Chem. Lab. Med. 45, 611–614. https://doi.org/10.1515/CCLM.2007.132 (2007).
doi: 10.1515/CCLM.2007.132 pubmed: 17484621
Wang, Q. L. et al. Association of HLA diversity with the risk of 25 cancers in the UK Biobank. EBioMedicine 92, 104588. https://doi.org/10.1016/j.ebiom.2023.104588 (2023).
doi: 10.1016/j.ebiom.2023.104588 pubmed: 37148584 pmcid: 10189092
Jones, M. R., Kamara, D., Karlan, B. Y., Pharoah, P. D. P. & Gayther, S. A. Genetic epidemiology of ovarian cancer and prospects for polygenic risk prediction. Gynecol Oncol 147, 705–713. https://doi.org/10.1016/j.ygyno.2017.10.001 (2017).
doi: 10.1016/j.ygyno.2017.10.001 pubmed: 29054568
Kar, S. P. et al. Common genetic variation and susceptibility to ovarian cancer: Current insights and future directions. Cancer Epidemiol. Biomarkers Prev 27, 395–404. https://doi.org/10.1158/1055-9965.EPI-17-0315 (2018).
doi: 10.1158/1055-9965.EPI-17-0315 pubmed: 28615364
Struzinska, I. et al. Somatic genomic and transcriptomic characterization of primary ovarian serous borderline tumors and low-grade serous carcinomas. J. Mol. Diagn. https://doi.org/10.1016/j.jmoldx.2023.12.004 (2024).
doi: 10.1016/j.jmoldx.2023.12.004 pubmed: 38280423
Qing, T. et al. Germline variant burden in cancer genes correlates with age at diagnosis and somatic mutation burden. Nat. Commun. 11, 2438. https://doi.org/10.1038/s41467-020-16293-7 (2020).
doi: 10.1038/s41467-020-16293-7 pubmed: 32415133 pmcid: 7228928
Chan, J. K. et al. Ovarian cancer in younger vs older women: A population-based analysis. Br. J. Cancer 95, 1314–1320. https://doi.org/10.1038/sj.bjc.6603457 (2006).
doi: 10.1038/sj.bjc.6603457 pubmed: 17088903 pmcid: 2360593
Gockley, A. et al. Outcomes of women with high-grade and low-grade advanced-stage serous epithelial ovarian cancer. Obstet. Gynecol. 129, 439–447. https://doi.org/10.1097/AOG.0000000000001867 (2017).
doi: 10.1097/AOG.0000000000001867 pubmed: 28178043 pmcid: 5328143
Gershenson, D. M. et al. Impact of age and primary disease site on outcome in women with low-grade serous carcinoma of the ovary or peritoneum: Results of a large single-institution registry of a rare tumor. J. Clin. Oncol. 33, 2675–2682. https://doi.org/10.1200/JCO.2015.61.0873 (2015).
doi: 10.1200/JCO.2015.61.0873 pubmed: 26195696 pmcid: 4534528

Auteurs

Klara Horackova (K)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Petra Zemankova (P)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.
Institute of Pathological Physiology, First Faculty of Medicine, Charles University, Prague, Czech Republic.

Petr Nehasil (P)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.
Institute of Pathological Physiology, First Faculty of Medicine, Charles University, Prague, Czech Republic.
Department of Paediatrics and Inherited Metabolic Disorders, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Michal Vocka (M)

Department of Oncology, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Milena Hovhannisyan (M)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Katerina Matejkova (K)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.
Department of Genetics and Microbiology, Faculty of Science, Charles University in Prague, Prague, Czech Republic.

Marketa Janatova (M)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Marta Cerna (M)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Petra Kleiblova (P)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.
Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Sandra Jelinkova (S)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Barbora Stastna (B)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.
Department of Biochemistry, Faculty of Science, Charles University, Prague, Czech Republic.

Pavel Just (P)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Tatana Dolezalova (T)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Barbora Nemcova (B)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Marketa Urbanova (M)

Centre for Medical Genetics and Reproductive Medicine, GENNET, Prague, Czech Republic.

Monika Koudova (M)

Centre for Medical Genetics and Reproductive Medicine, GENNET, Prague, Czech Republic.

Jana Hazova (J)

Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, Brno, Czech Republic.

Eva Machackova (E)

Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, Brno, Czech Republic.

Lenka Foretova (L)

Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, Brno, Czech Republic.

Viktor Stranecky (V)

Department of Paediatrics and Inherited Metabolic Disorders, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.

Michal Zikan (M)

Department of Gynecology and Obstetrics, Bulovka University Hospital and First Faculty of Medicine, Charles University, Prague, Czech Republic.

Zdenek Kleibl (Z)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic.
Institute of Pathological Physiology, First Faculty of Medicine, Charles University, Prague, Czech Republic.

Jana Soukupova (J)

Institute of Medical Biochemistry and Laboratory Diagnostics, First Faculty of Medicine, Charles University and General University Hospital in Prague, Prague, Czech Republic. jana.soukupova@lf1.cuni.cz.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH