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Nat Rev Cancer. 2017 Oct;17(10):605-619. doi: 10.1038/nrc.2017.69. Epub 2017 Sep 15.

Classifying the evolutionary and ecological features of neoplasms.

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Virginia G. Piper Center for Personalized Diagnostics, Biodesign Institute, Arizona State University, 1001 S. McAllister Ave, Tempe, Arizona 85287, USA.
Department of Psychology, Center for Evolution and Medicine, Arizona State University, 651 E. University Drive, Tempe, Arizona 85287, USA.
Evolution and Cancer Laboratory, Centre for Tumour Biology, Barts Cancer Institute, Queen Mary University of London, Charterhouse Square, London EC1M 6BQ, UK.
Centre for Evolution and Cancer, The Institute of Cancer Research, 15 Cotswold Road, Sutton, London SM2 5NG, UK.
Department of Anthropology, University of California Santa Barbara, Santa Barbara, California 93106, USA.
Department of Medical Oncology, Dana-Farber Cancer Institute, 450 Brookline Avenue D740C, Boston, Massachusetts 02215, USA.
Department of Cancer Imaging and Metabolism, Moffitt Cancer Center and Research Institute, 12902 Magnolia Drive, Tampa, Florida 33612, USA.
Centre for Evolution and Cancer, Division of Molecular Pathology, The Institute of Cancer Research, 237 Fulham Road, London SW3 6JB, UK.
Brady Urological Institute, The Johns Hopkins School of Medicine, 600 N. Wolfe Street, Baltimore, Maryland 21287, USA.
Cancer Biology and Evolution Program, Moffitt Cancer Center, 12902 Magnolia Drive, Tampa, Florida 33612, USA.
Cancer Research UK Lung Cancer Centre of Excellence, University College London Cancer Institute, Paul O'Gorman Building, 72 Huntley Street, London WC1E 6BT, UK.
Department of Biochemistry, Genetics and Immunology and Biomedical Research Center (CINBIO), University of Vigo, Spain; Galicia Sur Health Research Institute, Vigo, 36310, Spain.
Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA.
Departments of Pediatrics and Oncological Sciences, Huntsman Cancer Institute, University of Utah, 2000 Circle of Hope, Salt Lake City, Utah 84108, USA.
Department of Surgery, Duke University and Duke Cancer Institute, 465 Seeley Mudd Building, Durham, North Carolina 27710, USA.
Integrated Mathematical Oncology Department, Moffitt Cancer Center, 12902 Magnolia Drive, Tampa, Florida 33612, USA.
Department of Pathology, Norris Comprehensive Cancer Center, University of Southern California, 1441 Eastlake Avenue, NOR2424, Los Angeles, California 90033, USA.


Neoplasms change over time through a process of cell-level evolution, driven by genetic and epigenetic alterations. However, the ecology of the microenvironment of a neoplastic cell determines which changes provide adaptive benefits. There is widespread recognition of the importance of these evolutionary and ecological processes in cancer, but to date, no system has been proposed for drawing clinically relevant distinctions between how different tumours are evolving. On the basis of a consensus conference of experts in the fields of cancer evolution and cancer ecology, we propose a framework for classifying tumours that is based on four relevant components. These are the diversity of neoplastic cells (intratumoural heterogeneity) and changes over time in that diversity, which make up an evolutionary index (Evo-index), as well as the hazards to neoplastic cell survival and the resources available to neoplastic cells, which make up an ecological index (Eco-index). We review evidence demonstrating the importance of each of these factors and describe multiple methods that can be used to measure them. Development of this classification system holds promise for enabling clinicians to personalize optimal interventions based on the evolvability of the patient's tumour. The Evo- and Eco-indices provide a common lexicon for communicating about how neoplasms change in response to interventions, with potential implications for clinical trials, personalized medicine and basic cancer research.

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