Going to extremes: determinants of extraordinary response and survival in patients with cancer.
Journal
Nature reviews. Cancer
ISSN: 1474-1768
Titre abrégé: Nat Rev Cancer
Pays: England
ID NLM: 101124168
Informations de publication
Date de publication:
06 2019
06 2019
Historique:
pubmed:
12
5
2019
medline:
5
7
2019
entrez:
12
5
2019
Statut:
ppublish
Résumé
Research into factors affecting treatment response or survival in patients with cancer frequently involves cohorts that span the most common range of clinical outcomes, as such patients are most readily available for study. However, attention has turned to highly unusual patients who have exceptionally favourable or atypically poor responses to treatment and/or overall survival, with the expectation that patients at the extremes may provide insights that could ultimately improve the outcome of individuals with more typical disease trajectories. While clinicians can often recount surprising patients whose clinical journey was very unusual, given known clinical characteristics and prognostic indicators, there is a lack of consensus among researchers on how best to define exceptional patients, and little has been proposed for the optimal design of studies to identify factors that dictate unusual outcome. In this Opinion article, we review different approaches to identifying exceptional patients with cancer and possible study designs to investigate extraordinary clinical outcomes. We discuss pitfalls with finding these rare patients, including challenges associated with accrual of patients across different treatment centres and time periods. We describe recent molecular and immunological factors that have been identified as contributing to unusual patient outcome and make recommendations for future studies on these intriguing patients.
Identifiants
pubmed: 31076661
doi: 10.1038/s41568-019-0145-5
pii: 10.1038/s41568-019-0145-5
pmc: PMC7255796
mid: NIHMS1589093
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
339-348Subventions
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NCI NIH HHS
ID : U54 CA209978
Pays : United States
Références
Bateson, W. The Methods and Scope of Genetics (Cambridge Univ. Press, 1908).
Schwaederle, M. et al. Impact of precision medicine in diverse cancers: a meta-analysis of phase II clinical trials. J. Clin. Oncol. 33, 3817–3825 (2015).
doi: 10.1200/JCO.2015.61.5997
pubmed: 26304871
pmcid: 4737863
Takebe, N., McShane, L. & Conley, B. Biomarkers: exceptional responders-discovering predictive biomarkers. Nat. Rev. Clin. Oncol. 12, 132–134 (2015).
doi: 10.1038/nrclinonc.2015.19
pubmed: 25687910
Weinberg, R. A. The Biology of Cancer 2nd edn (Garland Science, 2014).
Printz, C. NCI launches exceptional responders initiative: researchers will attempt to identify why some patients respond to treatment so much better than others. Cancer 121, 803–804 (2015).
doi: 10.1002/cncr.29311
pubmed: 25739575
Chang, D. K. et al. Mining the genomes of exceptional responders. Nat. Rev. Cancer 14, 291–292 (2014).
doi: 10.1038/nrc3723
pubmed: 25688402
De La Torre, K. et al. Moonshots and metastatic disease: the need for a multi-faceted approach when studying atypical responses. NPJ Breast Cancer 3, 7 (2017).
doi: 10.1038/s41523-017-0010-1
Eisenhauer, E. A. et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer 45, 228–247 (2009).
doi: 10.1016/j.ejca.2008.10.026
pubmed: 19097774
Seymour, L. et al. iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics. Lancet Oncol. 18, e143–e152 (2017).
doi: 10.1016/S1470-2045(17)30074-8
pubmed: 28271869
pmcid: 5648544
Rustin, G. J. et al. Definitions for response and progression in ovarian cancer clinical trials incorporating RECIST 1.1 and CA 125 agreed by the Gynecological Cancer Intergroup (GCIG). Int. J. Gynecol. Cancer 21, 419–423 (2011).
doi: 10.1097/IGC.0b013e3182070f17
pubmed: 21270624
Loaiza-Bonilla, A. et al. Dramatic response to dabrafenib and trametinib combination in a BRAF V600E-mutated cholangiocarcinoma: implementation of a molecular tumour board and next-generation sequencing for personalized medicine. Ecancermedicalscience 8, 479 (2014).
doi: 10.3332/ecancer.2014.479
pubmed: 25435907
pmcid: 4239128
Colton, B. et al. Exceptional response to systemic therapy in advanced metastatic gastric cancer: a case report. Cureus 8, e457 (2016).
pubmed: 26918225
pmcid: 4752374
Heyman, J. & Leiter, E. Dramatic response of pulmonary metastasis from prostatic cancer to LH-RH agonist treatment. Mt Sinai J. Med. 56, 108–110 (1989).
pubmed: 2501670
Iyer, G. et al. Genome sequencing identifies a basis for everolimus sensitivity. Science 338, 221 (2012).
doi: 10.1126/science.1226344
pubmed: 22923433
pmcid: 3633467
Milowsky, M. I. et al. Phase II study of everolimus in metastatic urothelial cancer. BJU Int. 112, 462–470 (2013).
doi: 10.1111/j.1464-410X.2012.11720.x
pubmed: 23551593
pmcid: 4020005
Cantero, D. et al. Molecular study of long-term survivors of glioblastoma by gene-targeted next-generation sequencing. J. Neuropathol. Exp. Neurol. 77, 710–716 (2018).
doi: 10.1093/jnen/nly048
pubmed: 30010995
Garsed, D. W. et al. Homologous recombination DNA repair pathway disruption and retinoblastoma protein loss are associated with exceptional survival in high-grade serous ovarian cancer. Clin. Cancer Res. 24, 569–580 (2017).
doi: 10.1158/1078-0432.CCR-17-1621
pubmed: 29061645
Jimenez-Sanchez, A. et al. Heterogeneous tumor-immune microenvironments among differentially growing metastases in an ovarian cancer patient. Cell 170, 927–938 (2017).
doi: 10.1016/j.cell.2017.07.025
pubmed: 28841418
pmcid: 5589211
University of Michigan School of Public Health. Multidisciplinary Ovarian Cancer Outcomes Group. UMich https://sph.umich.edu/mocog/index.html (2018).
Sud, A., Kinnersley, B. & Houlston, R. S. Genome-wide association studies of cancer: current insights and future perspectives. Nat. Rev. Cancer 17, 692–704 (2017).
doi: 10.1038/nrc.2017.82
pubmed: 29026206
Kobel, M. et al. An immunohistochemical algorithm for ovarian carcinoma typing. Int. J. Gynecol. Pathol. 35, 430–441 (2016).
doi: 10.1097/PGP.0000000000000274
pubmed: 26974996
pmcid: 4978603
National Cancer Intelligence Network. Overview of Ovarian Cancer in England: Incidence, Mortality and Survival (National Health Service, 2012).
Ma, H., Sun, H. & Sun, X. Survival improvement by decade of patients aged 0–14 years with acute lymphoblastic leukemia: a SEER analysis. Sci. Rep. 4, 4227 (2014).
doi: 10.1038/srep04227
pubmed: 24572378
pmcid: 3936227
Aletti, G. D. et al. Ovarian cancer surgical resectability: relative impact of disease, patient status, and surgeon. Gynecol. Oncol. 100, 33–37 (2006).
doi: 10.1016/j.ygyno.2005.07.123
pubmed: 16153692
Parachoniak, C. A. et al. Exceptional durable response to everolimus in a patient with biphenotypic breast cancer harboring an STK11 variant. Cold Spring Harb. Mol. Case Stud. 3, a000778 (2017).
doi: 10.1101/mcs.a000778
pubmed: 28550065
pmcid: 5593157
Wagle, N. et al. Activating mTOR mutations in a patient with an extraordinary response on a phase I trial of everolimus and pazopanib. Cancer Discov. 4, 546–553 (2014).
doi: 10.1158/2159-8290.CD-13-0353
pubmed: 24625776
pmcid: 4122326
Ali, S. M. et al. Exceptional response on addition of everolimus to taxane in urothelial carcinoma bearing an NF2 mutation. Eur. Urol. 67, 1195–1196 (2015).
doi: 10.1016/j.eururo.2015.01.015
pubmed: 25630452
Wagle, N. et al. Response and acquired resistance to everolimus in anaplastic thyroid cancer. N. Engl. J. Med. 371, 1426–1433 (2014).
doi: 10.1056/NEJMoa1403352
pubmed: 25295501
pmcid: 4564868
Moujaber, T. et al. BRAF mutations in low-grade serous ovarian cancer and response to BRAF inhibition. JCO Precis. Oncol. https://doi.org/10.1200/PO.17.00221 (2018).
doi: 10.1200/PO.17.00221
McEvoy, C. R. et al. Profound MEK inhibitor response in a cutaneous melanoma harboring a GOLGA4-RAF1 fusion. J. Clin. Invest. 130, 123089 (2019).
pubmed: 30835257
Grisham, R. N. et al. Extreme outlier analysis identifies occult mitogen-activated protein kinase pathway mutations in patients with low-grade serous ovarian cancer. J. Clin. Oncol. 33, 4099–4105 (2015).
doi: 10.1200/JCO.2015.62.4726
pubmed: 26324360
pmcid: 4669594
Mehnert, J. M. et al. Immune activation and response to pembrolizumab in POLE-mutant endometrial cancer. J. Clin. Invest. 126, 2334–2340 (2016).
doi: 10.1172/JCI84940
pubmed: 27159395
pmcid: 4887167
Erson-Omay, E. Z. et al. Somatic POLE mutations cause an ultramutated giant cell high-grade glioma subtype with better prognosis. Neuro Oncol. 17, 1356–1364 (2015).
doi: 10.1093/neuonc/nov027
pubmed: 25740784
pmcid: 4578578
Stewart, C. J. et al. Long-term survival of patients with mismatch repair protein-deficient, high-stage ovarian clear cell carcinoma. Histopathology 70, 309–313 (2017).
doi: 10.1111/his.13040
pubmed: 27442838
Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 474, 609–615 (2011).
doi: 10.1038/nature10166
Patch, A.-M. et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature 521, 489–494 (2015).
doi: 10.1038/nature14410
pubmed: 26017449
Levin, M. K. et al. Genomic alterations in DNA repair and chromatin remodeling genes in estrogen receptor-positive metastatic breast cancer patients with exceptional responses to capecitabine. Cancer Med. 4, 1289–1293 (2015).
doi: 10.1002/cam4.464
pubmed: 25871911
pmcid: 4559040
Bolton, K. L. et al. Association between BRCA1 and BRCA2 mutations and survival in women with invasive epithelial ovarian cancer. JAMA 307, 382–390 (2012).
doi: 10.1001/jama.2012.20
pubmed: 22274685
pmcid: 3727895
Candido-dos-Reis, F. J. et al. Germline mutation in BRCA1 or BRCA2 and ten-year survival for women diagnosed with epithelial ovarian cancer. Clin. Cancer Res. 21, 652–657 (2015).
doi: 10.1158/1078-0432.CCR-14-2497
pubmed: 25398451
Kotsopoulos, J. et al. Ten-year survival after epithelial ovarian cancer is not associated with BRCA mutation status. Gynecol. Oncol. 140, 42–47 (2016).
doi: 10.1016/j.ygyno.2015.11.009
pubmed: 26556769
Maxwell, K. N. et al. BRCA locus-specific loss of heterozygosity in germline BRCA1 and BRCA2 carriers. Nat. Commun. 8, 319 (2017).
doi: 10.1038/s41467-017-00388-9
pubmed: 28831036
pmcid: 5567274
Wang, Y. et al. The BRCA1-delta11q alternative splice isoform bypasses germline mutations and promotes therapeutic resistance to PARP inhibition and cisplatin. Cancer Res. 76, 2778–2790 (2016).
doi: 10.1158/0008-5472.CAN-16-0186
pubmed: 27197267
pmcid: 4874568
Kondrashova, O. et al. Methylation of all BRCA1 copies predicts response to the PARP inhibitor rucaparib in ovarian carcinoma. Nat. Commun. 9, 3970 (2018).
doi: 10.1038/s41467-018-05564-z
pubmed: 30266954
pmcid: 6162272
Alsop, K. et al. BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian Ovarian Cancer Study Group. J. Clin. Oncol. 30, 2654–2663 (2012).
doi: 10.1200/JCO.2011.39.8545
pubmed: 22711857
pmcid: 3413277
Farmer, H. et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434, 917–921 (2005).
doi: 10.1038/nature03445
Bryant, H. E. et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434, 913–917 (2005).
doi: 10.1038/nature03443
Necchi, A. et al. Exceptional response to olaparib in BRCA2-altered urothelial carcinoma after PD-L1 inhibitor and chemotherapy failure. Eur. J. Cancer 96, 128–130 (2018).
doi: 10.1016/j.ejca.2018.03.021
pubmed: 29680362
Lheureux, S. et al. Long-term responders on olaparib maintenance in high-grade serous ovarian cancer: clinical and molecular characterization. Clin. Cancer Res. 23, 4086–4094 (2017).
doi: 10.1158/1078-0432.CCR-16-2615
pubmed: 28223274
Fridman, W. H. et al. The immune contexture in cancer prognosis and treatment. Nat. Rev. Clin. Oncol. 14, 717–734 (2017).
doi: 10.1038/nrclinonc.2017.101
pubmed: 28741618
pmcid: 28741618
Milne, K. et al. Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PLOS ONE 4, e6412 (2009).
doi: 10.1371/journal.pone.0006412
pubmed: 19641607
pmcid: 2712762
Webb, J. R., Milne, K. & Nelson, B. H. PD-1 and CD103 are widely coexpressed on prognostically favorable intraepithelial CD8 T cells in human ovarian cancer. Cancer Immunol. Res. 3, 926–935 (2015).
doi: 10.1158/2326-6066.CIR-14-0239
pubmed: 25957117
Djenidi, F. et al. CD8
doi: 10.4049/jimmunol.1402711
pubmed: 25725111
Wouters, M. C. A. & Nelson, B. H. Prognostic significance of tumor-infiltrating B cells and plasma cells in human cancer. Clin. Cancer Res. 24, 6125–6135 (2018).
doi: 10.1158/1078-0432.CCR-18-1481
pubmed: 30049748
pmcid: 30049748
Blank, C. U. et al. The “cancer immunogram”. Science 352, 658–660 (2016).
doi: 10.1126/science.aaf2834
pubmed: 27151852
Talhouk, A. et al. Molecular subtype not immune response drives outcomes in endometrial carcinoma. Clin. Cancer Res. https://doi.org/10.1158/1078-0432.CCR-18-3241 (2018).
doi: 10.1158/1078-0432.CCR-18-3241
pubmed: 30523022
Chen, D. S. & Mellman, I. Elements of cancer immunity and the cancer-immune set point. Nature 541, 321–330 (2017).
doi: 10.1038/nature21349
pubmed: 28102259
Lawrence, M. S. et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499, 214–218 (2013).
doi: 10.1038/nature12213
pubmed: 23770567
pmcid: 23770567
Yarchoan, M., Hopkins, A. & Jaffee, E. M. Tumor mutational burden and response rate to PD-1 inhibition. N. Engl. J. Med. 377, 2500–2501 (2017).
doi: 10.1056/NEJMc1713444
pubmed: 29262275
Le, D. T. et al. PD-1 blockade in tumors with mismatch-repair deficiency. N. Engl. J. Med. 372, 2509–2520 (2015).
doi: 10.1056/NEJMoa1500596
pubmed: 4481136
pmcid: 4481136
Overman, M. J. et al. Nivolumab in patients with metastatic DNA mismatch repair-deficient or microsatellite instability-high colorectal cancer (CheckMate 142): an open-label, multicentre, phase 2 study. Lancet Oncol. 18, 1182–1191 (2017).
doi: 10.1016/S1470-2045(17)30422-9
pubmed: 28734759
pmcid: 6207072
Le, D. T. et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science 357, 409–413 (2017).
doi: 10.1126/science.aan6733
pubmed: 28596308
pmcid: 5576142
Dunn, I. F. et al. Mismatch repair deficiency in high-grade meningioma: a rare but recurrent event associated with dramatic immune activation and clinical response to PD-1 blockade. JCO Precis. Oncol. https://doi.org/10.1200/po.18.00190 (2018).
doi: 10.1200/po.18.00190
pubmed: 30801050
pmcid: 6383717
Burr, M. L. et al. CMTM6 maintains the expression of PD-L1 and regulates anti-tumour immunity. Nature 549, 101–105 (2017).
doi: 10.1038/nature23643
pubmed: 28813417
pmcid: 5706633
Shi, Y. Regulatory mechanisms of PD-L1 expression in cancer cells. Cancer Immunol. Immunother. 67, 1481–1489 (2018).
doi: 10.1007/s00262-018-2226-9
pubmed: 30120503
George, J. et al. Genomic amplification of CD274 (PD-L1) in small-cell lung cancer. Clin. Cancer Res. 23, 1220–1226 (2017).
doi: 10.1158/1078-0432.CCR-16-1069
pubmed: 27620277
Chong, L. C. et al. Comprehensive characterization of programmed death ligand structural rearrangements in B cell non-Hodgkin lymphomas. Blood 128, 1206–1213 (2016).
doi: 10.1182/blood-2015-11-683003
pubmed: 27268263
Bellone, S. et al. Exceptional response to pembrolizumab in a metastatic, chemotherapy/radiation-resistant ovarian cancer patient harboring a PD-L1-genetic rearrangement. Clin. Cancer Res. 24, 3282–3291 (2018).
doi: 10.1158/1078-0432.CCR-17-1805
pubmed: 29351920
pmcid: 6050068
Goodman, A. M. et al. Prevalence of PDL1 amplification and preliminary response to immune checkpoint blockade in solid tumors. JAMA Oncol. 4, 1237–1244 (2018).
doi: 10.1001/jamaoncol.2018.1701
pubmed: 29902298
pmcid: 6139049
Green, M. R. et al. Integrative analysis reveals selective 9p24.1 amplification, increased PD-1 ligand expression, and further induction via JAK2 in nodular sclerosing Hodgkin lymphoma and primary mediastinal large B cell lymphoma. Blood 116, 3268–3277 (2010).
doi: 10.1182/blood-2010-05-282780
pubmed: 20628145
pmcid: 2995356
Amraee, A. et al. Efficacy of nivolumab as checkpoint inhibitor drug on survival rate of patients with relapsed/refractory classical Hodgkin lymphoma: a meta-analysis of prospective clinical study. Clin. Transl Oncol. https://doi.org/10.1007/s12094-018-02032-4 (2019).
doi: 10.1007/s12094-018-02032-4
pubmed: 30993647
Miao, D. et al. Genomic correlates of response to immune checkpoint therapies in clear cell renal cell carcinoma. Science 359, 801–806 (2018).
doi: 10.1126/science.aan5951
pubmed: 29301960
pmcid: 6035749
Jelinic, P. et al. Recurrent SMARCA4 mutations in small cell carcinoma of the ovary. Nat. Genet. 46, 424–426 (2014).
doi: 10.1038/ng.2922
pubmed: 24658004
pmcid: 5699446
Jelinic, P. et al. Immune-active microenvironment in small cell carcinoma of the ovary, hypercalcemic type: rationale for immune checkpoint blockade. J. Natl Cancer Inst. 110, 787–790 (2018).
doi: 10.1093/jnci/djx277
pubmed: 29365144
pmcid: 6037122
Gadducci, A. & Guerrieri, M. E. Immune checkpoint inhibitors in gynecological cancers: update of literature and perspectives of clinical research. Anticancer Res. 37, 5955–5965 (2017).
pubmed: 29061774
Wiegand, K. C. et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med. 363, 1532–1543 (2010).
doi: 10.1056/NEJMoa1008433
pubmed: 20942669
pmcid: 2976679
Champiat, S. et al. Hyperprogressive disease is a new pattern of progression in cancer patients treated by anti-PD-1/PD-L1. Clin. Cancer Res. 23, 1920–1928 (2017).
doi: 10.1158/1078-0432.CCR-16-1741
pubmed: 27827313
Kato, S. et al. Hyperprogressors after immunotherapy: analysis of genomic alterations associated with accelerated growth rate. Clin. Cancer Res. 23, 4242–4250 (2017).
doi: 10.1158/1078-0432.CCR-16-3133
pubmed: 28351930
pmcid: 5647162
Lo Russo, G. et al. Antibody-Fc/FcR interaction on macrophages as a mechanism for hyperprogressive disease in non-small cell lung cancer subsequent to PD-1/PD-L1 blockade. Clin. Cancer Res. 25, 989–999 (2019).
doi: 10.1158/1078-0432.CCR-18-1390
pubmed: 30206165
Tran, E. et al. Cancer immunotherapy based on mutation-specific CD4+T cells in a patient with epithelial cancer. Science 344, 641–645 (2014).
doi: 10.1126/science.1251102
Zacharakis, N. et al. Immune recognition of somatic mutations leading to complete durable regression in metastatic breast cancer. Nat. Med. 24, 724–730 (2018).
doi: 10.1038/s41591-018-0040-8
pubmed: 29867227
pmcid: 6348479
Maude, S. L. et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N. Engl. J. Med. 378, 439–448 (2018).
doi: 10.1056/NEJMoa1709866
pubmed: 29385370
pmcid: 5996391
Park, J. H. et al. Long-term follow-up of CD19 CAR therapy in acute lymphoblastic leukemia. N. Engl. J. Med. 378, 449–459 (2018).
doi: 10.1056/NEJMoa1709919
pubmed: 29385376
Mellman, I., Coukos, G. & Dranoff, G. Cancer immunotherapy comes of age. Nature 480, 480–489 (2011).
doi: 10.1038/nature10673
pubmed: 22193102
pmcid: 22193102
Sadelain, M., Riviere, I. & Riddell, S. Therapeutic T cell engineering. Nature 545, 423–431 (2017).
doi: 10.1038/nature22395
pubmed: 28541315
pmcid: 5632949
June, C. H. & Sadelain, M. Chimeric antigen receptor therapy. N. Engl. J. Med. 379, 64–73 (2018).
doi: 10.1056/NEJMra1706169
pubmed: 29972754
Fraietta, J. A. et al. Disruption of TET2 promotes the therapeutic efficacy of CD19-targeted T cells. Nature 558, 307–312 (2018).
doi: 10.1038/s41586-018-0178-z
pubmed: 29849141
pmcid: 6320248
Meyerhardt, J. A. et al. Dietary glycemic load and cancer recurrence and survival in patients with stage III colon cancer: findings from CALGB 89803. J. Natl Cancer Inst. 104, 1702–1711 (2012).
doi: 10.1093/jnci/djs399
pubmed: 23136358
pmcid: 3502194
Park, S. Y. et al. High-quality diets associate with reduced risk of colorectal cancer: analyses of diet quality indexes in the multiethnic cohort. Gastroenterology 153, 386–394 (2017).
doi: 10.1053/j.gastro.2017.04.004
pubmed: 28428143
pmcid: 5526717
Beasley, J. M. et al. Meeting the physical activity guidelines and survival after breast cancer: findings from the after breast cancer pooling project. Breast Cancer Res. Treat. 131, 637–643 (2012).
doi: 10.1007/s10549-011-1770-1
pubmed: 21935600
Campbell, P. T. et al. Associations of recreational physical activity and leisure time spent sitting with colorectal cancer survival. J. Clin. Oncol. 31, 876–885 (2013).
doi: 10.1200/JCO.2012.45.9735
pubmed: 23341510
Cannioto, R. A. et al. Recreational physical inactivity and mortality in women with invasive epithelial ovarian cancer: evidence from the Ovarian Cancer Association Consortium. Br. J. Cancer 115, 95–101 (2016).
doi: 10.1038/bjc.2016.153
pubmed: 27299959
pmcid: 4931371
Nagle, C. M. et al. Obesity and survival among women with ovarian cancer: results from the Ovarian Cancer Association Consortium. Br. J. Cancer 113, 817–826 (2015).
doi: 10.1038/bjc.2015.245
pubmed: 26151456
pmcid: 4559823
Nunez, C. et al. Physical activity, obesity and sedentary behaviour and the risks of colon and rectal cancers in the 45 and up study. BMC Public Health 18, 325 (2018).
doi: 10.1186/s12889-018-5225-z
pubmed: 29510753
pmcid: 5840833
Chan, J. A. et al. Hormone replacement therapy and survival after colorectal cancer diagnosis. J. Clin. Oncol. 24, 5680–5686 (2006).
doi: 10.1200/JCO.2006.08.0580
pubmed: 17179103
Symer, M. M. et al. Hormone replacement therapy and colorectal cancer incidence and mortality in the prostate, lung, colorectal, and ovarian cancer screening trial. Clin. Colorectal Cancer 17, e281–e288 (2018).
doi: 10.1016/j.clcc.2018.01.003
pubmed: 29398422
Eeles, R. A. et al. Adjuvant hormone therapy may improve survival in epithelial ovarian cancer: results of the AHT randomized trial. J. Clin. Oncol. 33, 4138–4144 (2015).
doi: 10.1200/JCO.2015.60.9719
pubmed: 26417001
Phipps, A. I. et al. Associations between cigarette smoking status and colon cancer prognosis among participants in North Central Cancer Treatment Group phase III trial N0147. J. Clin. Oncol. 31, 2016–2023 (2013).
doi: 10.1200/JCO.2012.46.2457
pubmed: 23547084
pmcid: 3661936
Praestegaard, C. et al. Cigarette smoking is associated with adverse survival among women with ovarian cancer: results from a pooled analysis of 19 studies. Int. J. Cancer 140, 2422–2435 (2017).
doi: 10.1002/ijc.30600
pubmed: 28063166
pmcid: 5489656
Jayasekara, H. et al. Associations of alcohol intake, smoking, physical activity and obesity with survival following colorectal cancer diagnosis by stage, anatomic site and tumor molecular subtype. Int. J. Cancer 142, 238–250 (2018).
doi: 10.1002/ijc.31049
pubmed: 28921583
Molina, Y. et al. Resilience among patients across the cancer continuum: diverse perspectives. Clin. J. Oncol. Nurs. 18, 93–101 (2014).
doi: 10.1188/14.CJON.93-101
pubmed: 24476731
pmcid: 4002224
Strauss, B. et al. The influence of resilience on fatigue in cancer patients undergoing radiation therapy (RT). J. Cancer Res. Clin. Oncol. 133, 511–518 (2007).
doi: 10.1007/s00432-007-0195-z
pubmed: 17576595
Wenzel, L. B. et al. Resilience, reflection, and residual stress in ovarian cancer survivorship: a gynecologic oncology group study. Psychooncology 11, 142–153 (2002).
doi: 10.1002/pon.567
pubmed: 11921330
Pearce, C. L. et al. Combined and interactive effects of environmental and GWAS-identified risk factors in ovarian cancer. Cancer Epidemiol. Biomarkers Prev. 22, 880–890 (2013).
doi: 10.1158/1055-9965.EPI-12-1030-T
pubmed: 23462924
pmcid: 3963289
Harvard Medical School Department of Biomedical Informatics. Network of Enigmatic Exceptional Responders (NEER) study. People-Powered Medicine https://peoplepoweredmedicine.org/neer (2018).
US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT02243592 (2019).
US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT02701907 (2018).
US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT03740503 (2018).
US National Library of Medicine. ClinicalTrials.gov https://clinicaltrials.gov/ct2/show/NCT02321735 (2016).