{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,17]],"date-time":"2026-07-17T05:58:43Z","timestamp":1784267923618,"version":"3.55.0"},"reference-count":53,"publisher":"Impact Journals, LLC","issue":"44","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Oncotarget"],"published-print":{"date-parts":[[2016,11,1]]},"DOI":"10.18632\/oncotarget.12106","type":"journal-article","created":{"date-parts":[[2016,9,23]],"date-time":"2016-09-23T22:08:14Z","timestamp":1474668494000},"page":"71123-71135","source":"Crossref","is-referenced-by-count":34,"title":["Similarity and diversity of the tumor microenvironment in multiple metastases: critical implications for overall and progression-free survival of high-grade serous ovarian cancer"],"prefix":"10.18632","volume":"7","author":[{"given":"Andreas","family":"Heindl","sequence":"first","affiliation":[{"name":"Centre for Evolution and Cancer, The Institute of Cancer Research, London, UK"},{"name":"Centre for Molecular Pathology, Royal Marsden Hospital, London, UK"},{"name":"Division of Molecular Pathology, The Institute of Cancer Research, London, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunyan","family":"Lan","sequence":"additional","affiliation":[{"name":"Department of Gynecologic Oncology, Sun Yat-sen University Cancer Centre, Guangzhou, China"},{"name":"State Key Laboratory of Oncology in South China, Collaborative Innovation Centre for Cancer Medicine, Guangzhou, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel Nava","family":"Rodrigues","sequence":"additional","affiliation":[{"name":"Division of Cancer Therapeutics, The Institute of Cancer Research, London, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Konrad","family":"Koelble","sequence":"additional","affiliation":[{"name":"Division of Molecular Pathology, The Institute of Cancer Research, London, UK"},{"name":"Department of Histopathology, Royal Marsden Hospital, London, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yinyin","family":"Yuan","sequence":"additional","affiliation":[{"name":"Centre for Evolution and Cancer, The Institute of Cancer Research, London, UK"},{"name":"Centre for Molecular Pathology, Royal Marsden Hospital, London, UK"},{"name":"Division of Molecular Pathology, The Institute of Cancer Research, London, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"7892","published-online":{"date-parts":[[2016,9,19]]},"reference":[{"key":"1","doi-asserted-by":"crossref","first-page":"5880","DOI":"10.1158\/0008-5472.CAN-09-4341","article-title":"Identification of a metalloprotease-chemokine signaling system in the ovarian cancer microenvironment: implications for antiangiogenic therapy","volume":"70","author":"Kuliopulos","year":"2010","journal-title":"Cancer Res"},{"key":"2","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1158\/1078-0432.CCR-12-2243","article-title":"New strategies in the treatment of ovarian cancer: current clinical perspectives and future potential","volume":"19","author":"Kaye","year":"2013","journal-title":"Clin Cancer Res"},{"key":"3","doi-asserted-by":"crossref","first-page":"20130020","DOI":"10.1098\/rsfs.2013.0020","article-title":"Exploiting ecological principles to better understand cancer progression and treatment","volume":"3","author":"Anderson","year":"2013","journal-title":"Interface Focus"},{"key":"4","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1002\/path.4230","article-title":"Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling","volume":"231","author":"Melnyk","year":"2013","journal-title":"J Pathol"},{"key":"5","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1038\/nrc2644","article-title":"The biology of ovarian cancer: new opportunities for translation","volume":"9","author":"Mills","year":"2009","journal-title":"Nat Rev Cancer"},{"key":"6","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1038\/nrc4019","article-title":"Rethinking ovarian cancer II: reducing mortality from high-grade serous ovarian cancer","volume":"15","author":"Martins","year":"2015","journal-title":"Nat Rev Cancer"},{"key":"7","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.1200\/JCO.2002.20.5.1248","article-title":"Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: A meta-analysis","volume":"20","author":"Montz","year":"2002","journal-title":"J Clin Oncol"},{"key":"8","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1097\/00006254-199507000-00012","article-title":"The Effect of Debulking Surgery After Induction Chemotherapy on the Prognosis in Advanced Epithelial Ovarian Cancer","volume":"50","author":"Pecorelli","year":"1995","journal-title":"Obstet Gynecol Surv"},{"key":"9","doi-asserted-by":"crossref","first-page":"2473","DOI":"10.1056\/NEJMoa1104390","article-title":"Incorporation of Bevacizumab in the Primary Treatment of Ovarian Cancer","volume":"365","author":"S","year":"2011","journal-title":"N Engl J Med"},{"key":"10","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.ygyno.2009.03.018","article-title":"Improved progression-free and overall survival in advanced ovarian cancer as a result of a change in surgical paradigm","volume":"114","author":"Barakat","year":"2009","journal-title":"Gynecol Oncol"},{"key":"11","doi-asserted-by":"crossref","first-page":"906","DOI":"10.1097\/IGC.0000000000000690","article-title":"Minimal Macroscopic Residual Disease (0. 1-1 cm). Is It Still a Surgical Goal in Advanced Ovarian Cancer?","volume":"26","author":"Gonzalez-Martin","year":"2016","journal-title":"Int J Gynecol Cancer"},{"key":"12","doi-asserted-by":"publisher","first-page":"18573","DOI":"10.18632\/oncotarget.7613","article-title":"Markers of fibroblast-rich tumor stroma and perivascular cells in serous ovarian cancer: inter- and intra-patient heterogeneity and impact on survival","volume":"7","author":"Dahlstrand","year":"2016","journal-title":"Oncotarget"},{"key":"13","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1111\/j.2517-6161.1972.tb00899.x","article-title":"Regression Models and Life-Tables","volume":"34","author":"Cox","year":"1972","journal-title":"J R Stat Soc Ser B"},{"key":"14","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1111\/eva.12031","article-title":"From forest and agro-ecosystems to the microecosystems of the human body: what can landscape ecology tell us about tumor growth, metastasis, and treatment options?","volume":"6","author":"Thomas","year":"2013","journal-title":"Evol Appl"},{"key":"15","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.critrevonc.2008.01.012","article-title":"New therapies for ovarian cancer: cytotoxics and molecularly targeted agents","volume":"67","author":"Awada","year":"2008","journal-title":"Crit Rev Oncol Hematol"},{"key":"16","first-page":"1","article-title":"Immunotherapy of Ovarian Cancer: The Role of Checkpoint Inhibitors","volume":"2015","author":"Panici","year":"2015","journal-title":"J Immunol Res"},{"key":"17","doi-asserted-by":"crossref","first-page":"7499","DOI":"10.1158\/0008-5472.CAN-09-1354","article-title":"Lessons from Applied Ecology: Cancer Control Using an Evolutionary Double Bind","volume":"69","author":"Vincent","year":"2009","journal-title":"Cancer Res"},{"key":"18","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1101\/gr.161026.113","article-title":"Genomic and transcriptomic plasticity in treatment-naive ovarian cancer","volume":"24","author":"van 't Slot","year":"2014","journal-title":"Genome Res"},{"key":"19","first-page":"71","article-title":"Cancer statistics, 2008","volume":"58","author":"Thun","journal-title":"CA Cancer J Clin"},{"key":"20","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1038\/nrc2618","article-title":"Microenvironmental regulation of metastasis","volume":"9","author":"Pollard","year":"2009","journal-title":"Nat Rev Cancer"},{"key":"21","unstructured":"Kaplan, Meier. Nonparametric Estimation from Incomplete Observations. J. Am. Stat. Assoc."},{"key":"22","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1097\/01.pas.0000213335.40358.47","article-title":"Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: Evidence for a causal relationship","volume":"31","author":"Crum","year":"2007","journal-title":"Am J Surg Pathol"},{"key":"23","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1038\/nrc3712","article-title":"Turning ecology and evolution against cancer","volume":"14","author":"Gore","year":"2014","journal-title":"Nat Rev Cancer"},{"key":"24","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1002\/path.3023","article-title":"TP53 mutations in serous tubal intraepithelial carcinoma and concurrent pelvic high-grade serous carcinoma\u2014evidence supporting the clonal relationship of the two lesions","volume":"226","author":"Shih","year":"2012","journal-title":"J Pathol"},{"key":"25","doi-asserted-by":"crossref","first-page":"16317","DOI":"10.1038\/srep16317","article-title":"Quantitative histology analysis of the ovarian tumour microenvironment","volume":"5","author":"Yuan","year":"2015","journal-title":"Sci Rep"},{"key":"26","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1002\/path.4536","article-title":"Efficient molecular subtype classification of high-grade serous ovarian cancer","volume":"236","author":"Bowtell","year":"2015","journal-title":"J Pathol"},{"key":"27","doi-asserted-by":"crossref","first-page":"625","DOI":"10.2741\/e275","article-title":"STICS, SCOUTs and p53 signatures; a new language for pelvic serous carcinogenesis","volume":"3","author":"Crum","year":"2011","journal-title":"Front Biosci (Elite Ed)"},{"key":"28","doi-asserted-by":"crossref","first-page":"3514","DOI":"10.1002\/ece3.1155","article-title":"Choosing and using diversity indices: insights for ecological applications from the German Biodiversity Exploratories","volume":"4","author":"Rillig","year":"2014","journal-title":"Ecol Evol"},{"key":"29","unstructured":"Murakami, Matsumura, Mandai, Yoshihara, Tanabe, Nakai, Yamanoi, Abiko, Yoshioka, Hamanishi, Yamaguchi, Baba, Koshiyama, et al. Establishment of a Novel Histopathological Classification of High-Grade Serous Ovarian Carcinoma Correlated with Prognostically Distinct Gene Expression Subtypes. Am. J. Pathol."},{"key":"30","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1038\/nrc1611","article-title":"Ovarian cancer metastasis: integrating insights from disparate model organisms","volume":"5","author":"Montell","year":"2005","journal-title":"Nat Rev Cancer"},{"key":"31","doi-asserted-by":"crossref","first-page":"e1001961","DOI":"10.1371\/journal.pmed.1001961","article-title":"Microenvironmental Heterogeneity Parallels Breast Cancer Progression: A Histology-Genomic Integration Analysis","volume":"13","author":"Yuan","year":"2016","journal-title":"PLOS Med"},{"key":"32","unstructured":"Nawaz, Yuan. Computational pathology: Exploring the spatial dimension of tumor ecology. Cancer Lett."},{"key":"33","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1038\/nature10166","article-title":"Integrated genomic analyses of ovarian carcinoma","volume":"474","author":"Network TCGAR","year":"2011","journal-title":"Nature"},{"key":"34","first-page":"98","article-title":"The distribution of secondary growths in cancer of the breast. 1889","volume":"8","author":"Paget","year":"1989","journal-title":"Cancer Metastasis Rev"},{"key":"35","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1172\/JCI40724","article-title":"Cellular and genetic diversity in the progression of in situ human breast carcinomas to an invasive phenotype","volume":"120","author":"Polyak","year":"2010","journal-title":"J Clin Invest"},{"key":"36","first-page":"74","article-title":"Global cancer statistics, 2002","volume":"55","author":"Pisani","journal-title":"CA Cancer J Clin"},{"key":"37","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1016\/j.ccr.2013.10.013","article-title":"Transformation of the fallopian tube secretory epithelium leads to high-grade serous ovarian cancer in Brca;Tp53;Pten models","volume":"24","author":"Drapkin","year":"2013","journal-title":"Cancer Cell"},{"key":"38","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1093\/jnci\/92.9.699","article-title":"Randomized intergroup trial of cisplatin-paclitaxelcisplatin-cyclophosphamide in women with advanced epithelial ovarian cancer: three-year results","volume":"92","author":"Swenerton","year":"2000","journal-title":"J Natl Cancer Inst"},{"key":"39","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1002\/path.1000","article-title":"Dysplastic changes in prophylactically removed Fallopian tubes of women predisposed to developing ovarian cancer","volume":"195","author":"Verheijen","year":"2001","journal-title":"J Pathol"},{"key":"40","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1593\/tlo.08178","article-title":"Ecological therapy for cancer: defining tumors using an ecosystem paradigm suggests new opportunities for novel cancer treatments","volume":"1","author":"Axelrod","year":"2008","journal-title":"Transl Oncol"},{"key":"41","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1038\/nrc2621","article-title":"The metastatic niche: adapting the foreign soil","volume":"9","author":"Lyden","year":"2009","journal-title":"Nat Rev Cancer"},{"key":"42","doi-asserted-by":"crossref","first-page":"1718","DOI":"10.1080\/13658816.2015.1059433","article-title":"Handbook of spatial point-pattern analysis in ecology","volume":"29","author":"Rosenberg","year":"2015","journal-title":"Int J Geogr Inf Sci"},{"key":"43","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1007\/s00404-014-3446-7","article-title":"Success rate and safety of tumor debulking with diaphragmatic surgery for advanced epithelial ovarian cancer and peritoneal cancer","volume":"291","author":"Okamoto","year":"2015","journal-title":"Arch Gynecol Obstet"},{"key":"44","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.maturitas.2013.11.009","article-title":"New perspectives in ovarian cancer treatment","volume":"77","author":"Oehler","year":"2014","journal-title":"Maturitas"},{"key":"45","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1145\/584091.584093","article-title":"A mathematical theory of communication","volume":"5","author":"Shannon","year":"2001","journal-title":"ACM SIGMOBILE Mob Comput Commun Rev"},{"key":"46","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1038\/163688a0","article-title":"Measurement of Diversity","volume":"163","author":"Simpson","year":"1949","journal-title":"Nature"},{"key":"47","doi-asserted-by":"crossref","first-page":"403","DOI":"10.2217\/fon.12.22","article-title":"Bevacizumab and breast cancer: what does the future hold?","volume":"8","author":"Takabe","year":"2012","journal-title":"Future Oncol"},{"key":"48","doi-asserted-by":"crossref","first-page":"5198","DOI":"10.1158\/1078-0432.CCR-08-0196","article-title":"Novel Molecular Subtypes of Serous and Endometrioid Ovarian Cancer Linked to Clinical Outcome","volume":"14","author":"Chiew","year":"2008","journal-title":"Clin Cancer Res"},{"key":"49","first-page":"517","article-title":"Prognostically relevant gene signatures of high-grade serous ovarian carcinoma","volume":"123","author":"Saksena","year":"2013","journal-title":"J Clin Invest"},{"key":"50","doi-asserted-by":"crossref","first-page":"3621","DOI":"10.1200\/JCO.2006.10.2517","article-title":"Prognostic factors for stage III epithelial ovarian cancer: a Gynecologic Oncology Group Study","volume":"25","author":"McGuire","year":"2007","journal-title":"J Clin Oncol"},{"key":"51","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1038\/nrc2583","article-title":"Beyond chemotherapy: targeted therapies in ovarian cancer","volume":"9","author":"Kaye","year":"2009","journal-title":"Nat Rev Cancer"},{"key":"52","doi-asserted-by":"crossref","first-page":"5016","DOI":"10.1158\/0008-5472.CAN-13-0023","article-title":"TGF- Modulates Ovarian Cancer Invasion by Upregulating CAF-Derived Versican in the Tumor Microenvironment","volume":"73","author":"Mok","year":"2013","journal-title":"Cancer Res"},{"key":"53","first-page":"157ra143","article-title":"Quantitative image analysis of cellular heterogeneity in breast tumors complements genomic profiling","volume":"4","author":"Markowetz","year":"2012","journal-title":"Sci Transl Med"}],"container-title":["Oncotarget"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.oncotarget.com\/lookup\/doi\/10.18632\/oncotarget.12106","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,19]],"date-time":"2024-06-19T15:25:03Z","timestamp":1718810703000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.oncotarget.com\/lookup\/doi\/10.18632\/oncotarget.12106"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,9,19]]},"references-count":53,"journal-issue":{"issue":"44","published-print":{"date-parts":[[2016,11,1]]}},"alternative-id":["12106","27661102"],"URL":"https:\/\/doi.org\/10.18632\/oncotarget.12106","relation":{},"ISSN":["1949-2553"],"issn-type":[{"value":"1949-2553","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,9,19]]}}}