Nonlinear adaptive control of competitive release and chemotherapeutic resistance.

We use a three-component replicator system with healthy cells, sensitive cells, and resistant cells, with a prisoner's dilemma payoff matrix from evolutionary game theory, to model and control the nonlinear dynamical system governing the ecological mechanism of competitive release by which tumors develop chemotherapeutic resistance. The control method we describe is based on nonlinear trajectory design and energy transfer methods first introduced in the orbital mechanics literature for Hamiltonian systems. For continuous therapy, the basin boundaries of attraction associated with the chemo-sensitive population and the chemo-resistant population for increasing values of chemo-concentrations have an intertwined spiral structure with extreme sensitivity to changes in chemo-concentration level as well as sensitivity with respect to resistant mutations. For time-dependent therapies, we introduce an orbit transfer method to construct continuous families of periodic (closed) orbits by switching the chemo-dose at carefully chosen times and appropriate levels to design schedules that are superior to both maximum tolerated dose (MTD) schedules and low-dose metronomic (LDM) schedules, both of which ultimately lead to fixation of sensitive cells or resistant cells. By keeping the three subpopulations of cells in competition with each other indefinitely, we avoid fixation of the cancer cell population and regrowth of a resistant tumor. The method can be viewed as a way to dynamically shape the average population fitness landscape of a tumor to steer the chemotherapeutic response curve. We show that the method is remarkably insensitive to initial conditions and small changes in chemo-dosages, an important criterion for turning the method into an actionable strategy.

[1]  Robert Gatenby,et al.  Opinion: Control vs. eradication: Applying infectious disease treatment strategies to cancer , 2015, Proceedings of the National Academy of Sciences.

[2]  Paul Jaffe,et al.  Orbital mechanics , 2017, IEEE Spectrum.

[3]  Jeffrey West,et al.  The prisoner's dilemma as a cancer model. , 2015, Convergent science physical oncology.

[4]  Dominik Wodarz,et al.  Drug resistance in cancer: principles of emergence and prevention. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Ville Mustonen,et al.  The value of monitoring to control evolving populations , 2014, Proceedings of the National Academy of Sciences.

[6]  R. Gatenby A change of strategy in the war on cancer , 2009, Nature.

[7]  M. Perry The Chemotherapy Source Book , 1992, Annals of Internal Medicine.

[8]  Troy Day,et al.  The evolution of drug resistance and the curious orthodoxy of aggressive chemotherapy , 2011, Proceedings of the National Academy of Sciences.

[9]  P. Newton,et al.  Chemotherapeutic Dose Scheduling Based on Tumor Growth Rates Provides a Case for Low-Dose Metronomic High-Entropy Therapies. , 2017, Cancer research.

[10]  David Basanta,et al.  Exploiting ecological principles to better understand cancer progression and treatment , 2013, Interface Focus.

[11]  Alexander G. Fletcher,et al.  Steering Evolution with Sequential Therapy to Prevent the Emergence of Bacterial Antibiotic Resistance , 2015, PLoS Comput. Biol..

[12]  Jacob G. Scott,et al.  Optimal Therapy Scheduling Based on a Pair of Collaterally Sensitive Drugs , 2017, Bulletin of Mathematical Biology.

[13]  Ericka Stricklin-Parker,et al.  Ann , 2005 .

[14]  Josef Hofbauer,et al.  Evolutionary Games and Population Dynamics , 1998 .

[15]  Chen-Hsiang Yeang,et al.  Impact of genetic dynamics and single-cell heterogeneity on development of nonstandard personalized medicine strategies for cancer , 2012, Proceedings of the National Academy of Sciences.

[16]  Paul K. Newton,et al.  An Evolutionary Model of Tumor Cell Kinetics and the Emergence of Molecular Heterogeneity Driving Gompertzian Growth , 2015, SIAM Rev..

[17]  Steven A. Rosenberg,et al.  Adoptive immunotherapy for cancer: harnessing the T cell response , 2012, Nature Reviews Immunology.

[18]  Joel s. Brown,et al.  The Evolution and Ecology of Resistance in Cancer Therapy. , 2018, Cold Spring Harbor perspectives in medicine.

[19]  Shane D. Ross,et al.  Connecting orbits and invariant manifolds in the spatial restricted three-body problem , 2004 .

[20]  B. Levin,et al.  The biological cost of antibiotic resistance. , 1999, Current opinion in microbiology.

[21]  L. Norton A Gompertzian model of human breast cancer growth. , 1988, Cancer research.

[22]  Frank Thuijsman,et al.  Spatial vs. non-spatial eco-evolutionary dynamics in a tumor growth model. , 2017, Journal of theoretical biology.

[23]  Robert A Gatenby,et al.  A theoretical quantitative model for evolution of cancer chemotherapy resistance , 2010, Biology Direct.

[24]  Shane D. Ross,et al.  Halo orbit mission correction maneuvers using optimal control , 2002, Autom..

[25]  K. Pienta,et al.  Evolution of cooperation among tumor cells , 2006, Proceedings of the National Academy of Sciences.

[26]  J. Connell The Influence of Interspecific Competition and Other Factors on the Distribution of the Barnacle Chthamalus Stellatus , 1961 .

[27]  Quantifying Competitive Exclusion and Competitive Release in Ecological Communities: A Conceptual Framework and a Case Study , 2016, PloS one.

[28]  C. Maley,et al.  Cancer is a disease of clonal evolution within the body1–3. This has profound clinical implications for neoplastic progression, cancer prevention and cancer therapy. Although the idea of cancer as an evolutionary problem , 2006 .

[29]  Joel s. Brown,et al.  Game theory as a conceptual framework for managing insect pests. , 2017, Current opinion in insect science.

[30]  Shane D. Ross,et al.  Multiple Gravity Assists, Capture, and Escape in the Restricted Three-Body Problem , 2007, SIAM J. Appl. Dyn. Syst..

[31]  Piyush Grover,et al.  Designing Trajectories in a Planet-Moon Environment Using the Controlled Keplerian Map , 2009 .

[32]  David Basanta,et al.  Exploiting evolution to treat drug resistance: combination therapy and the double bind. , 2011, Molecular pharmaceutics.

[33]  F. Gould The evolutionary potential of crop pests. , 1991 .

[34]  Shane D. Ross,et al.  Heteroclinic connections between periodic orbits and resonance transitions in celestial mechanics. , 2000, Chaos.

[35]  Carlo C. Maley,et al.  Overlooking Evolution: A Systematic Analysis of Cancer Relapse and Therapeutic Resistance Research , 2011, PloS one.

[36]  C. Hauert,et al.  Coevolutionary dynamics: from finite to infinite populations. , 2004, Physical review letters.

[37]  R. Lewontin The Units of Selection , 1970, The Structure and Confirmation of Evolutionary Theory.

[38]  Joel s. Brown,et al.  Integrating evolutionary dynamics into treatment of metastatic castrate-resistant prostate cancer , 2017, Nature Communications.

[39]  Camille Stephan-Otto Attolini,et al.  Evolutionary Theory of Cancer , 2009, Annals of the New York Academy of Sciences.

[40]  Sarah E Seton-Rogers,et al.  Chemotherapy: Preventing competitive release , 2016, Nature Reviews Cancer.

[41]  Michael C. Perry,et al.  American Society of Clinical Oncology educational book , 2003 .

[42]  R. Gillies,et al.  Exploiting evolutionary principles to prolong tumor control in preclinical models of breast cancer , 2016, Science Translational Medicine.