Mathematical modeling of glioma therapy using oncolytic viruses

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2013, 10(3): 565-578. doi: 10.3934/mbe.2013.10.565

Mathematical modeling of glioma therapy using oncolytic viruses

Baba Issa Camara ^1, , Houda Mokrani ^2, and Evans K. Afenya ^3,

1.	Laboratoire Interdisciplinaire des Environnements Continentaux, Université de Lorraine, CNRS UMR 7360, 8 rue du Général Delestraint, 57070 METZ, France
2.	Laboratoire de Mathématiques Raphaël Salem, Université de Rouen, UMR 6085 CNRS, Avenue de l'Université, 76801 Saint Etienne du Rouvray, France
3.	Department of Mathematics, Elmhurst College, 190 Prospect Avenue, Elmhurst, IL 60126, United States

Received June 2012 Revised February 2013 Published April 2013

Abstract
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Diffuse infiltrative gliomas are adjudged to be the most common primary brain tumors in adults and they tend to blend in extensively in the brain micro-environment. This makes it difficult for medical practitioners to successfully plan effective treatments. In attempts to prolong the lengths of survival times for patients with malignant brain tumors, novel therapeutic alternatives such as gene therapy with oncolytic viruses are currently being explored. Based on such approaches and existing work, a spatio-temporal model that describes interaction between tumor cells and oncolytic viruses is developed. Conditions that lead to optimal therapy in minimizing cancer cell proliferation and otherwise are analytically demonstrated. Numerical simulations are conducted with the aim of showing the impact of virotherapy on proliferation or invasion of cancer cells and of estimating survival times.

Keywords: Cancer gene therapy, mathematical model., oncolytic viruses.

Mathematics Subject Classification: Primary: 92C37, 35B35; Secondary: 35B4.

Citation: Baba Issa Camara, Houda Mokrani, Evans K. Afenya. Mathematical modeling of glioma therapy using oncolytic viruses. Mathematical Biosciences & Engineering, 2013, 10 (3) : 565-578. doi: 10.3934/mbe.2013.10.565

References:

[1]	E. C. Alvord Jr and C. M. Shaw, Neoplasms affecting the nervous system of the elderly, in "The Pathology of the Aging Human Nervous System" (ed. S. Duckett), Lea and Fabiger, Philadelphia, (1991), 210-286.
[2]	D. D. Barker and A. J. Berk, Adenovirus proteins from both E1B reading frames are required for transformation of rodent cells by viral infection and DNA transfection, Virology, 156 (1987), 107-121. doi: 10.1016/0042-6822(87)90441-7.
[3]	N. Bagheri, M. Shiina, D. A. Lauffenburger and W. M. Korn, A dynamical systems model for combinatorial cancer therapy enhances oncolytic adenovirus efficacy by MEK-Inhibition, PLoS Comput. Biol., 7 (2011), e1001085. doi: 10.1371/journal.pcbi.1001085.
[4]	F. G. Blankenberg, R. L. Teplitz, W. Ellis, M. S. Salamat, B. H. Min, L. Hall, D. B. Boothroyd, I. M. Johnstone and D. R. Enzmann, The influence of volumetric tumor doubling time, DNA ploidy, and histologic grade on the survival of patients with intracranial astrocytomas, AJNR Am. J. Neuroradiol, 16 (1995), 1001-1012.
[5]	P. C. Burger, E. R. Heinz, T. Shibata and P. Kleihues, Topographic anatomy and CT correlations in the untreated glioblastoma multiforme, J. Neurosurg, 68 (1988), 698-704. doi: 10.3171/jns.1988.68.5.0698.
[6]	B. I. Camara and H. Mokrani, Analysis of wave solutions of an adhenovirus-tumor cell system, Abstract and Applied Analysis, (ID 590326), (2012), 1-13. doi: 10.1155/2012/590326.
[7]	G. Cherubini, T. Petouchoff, M. Grossi, S. Piersanti, E. Cundari and I. Saggio, E1B55K-deleted adenovirus (ONYX-015) overrides G1/S and G2/M checkpoints and causes mitotic catastrophe and endoreduplication in p53-proficient normal cells, Cell Cycle, 5 (2006), 2244-2252.
[8]	An. Claes, A. J. Idema and P. Wesseling, Diffuse glioma growth: A guerilla war, Acta Neuropathol, 114 (2007), 443-458. doi: 10.1007/s00401-007-0293-7.
[9]	J. C. Concannon, S. Kramer S and R. Berry, The extent of intracranial gliomata at autopsy and its relation to techniques used in radiation therapy of brain tumors, Am. J. Roentgenol. Radium Ther. Nucl. Med., 84 (1960), 99-107.
[10]	L. K. Csatary, G. Gosztonyi, J. Szeberenyi, Z. Fabian, V. Liszka, B. Bodey and C. M. Csatary, MTH-68/H oncolytic viral treatment in human high-grade gliomas, J. Neurooncol, 67 (2004), 83-93. doi: 10.1023/B:NEON.0000021735.85511.05.
[11]	K. J. Excoffon, G. L. Traver and J. Zabner, The role of the extracellular domain in the biology of the coxsackievirus and adenovirus receptor, Am. J. Respir. Cell Mol. Biol., 32 (2005), 498-503. doi: 10.1165/rcmb.2005-0031OC.
[12]	E. Fan, Extended tanh-function method and its applications to nonlinear equations, Phys. Lett. A, 277 (2000), 212-218. doi: 10.1016/S0375-9601(00)00725-8.
[13]	A. Friedman and Y. Tao, Analysis of a model of a virus that replicates selectively in tumor cells, J. Math. Biol., 47 (2003), 391-423. doi: 10.1007/s00285-003-0199-5.
[14]	X. Ge and M. Arcak, A new sufficient condition for additive D-stability and application to cyclic reaction-diffusion models, American Control Conference, (2009), 2904-2909. doi: 10.1109/ACC.2009.5160022.
[15]	H. L. Harpold, E. C. Alvord Jr. and K. R. Swanson, The evolution of mathematical modeling of glioma proliferation and invasion, J. Neuropathol. Exp. Neurol., 66 (2007), 1-9. doi: 10.1097/nen.0b013e31802d9000.
[16]	D. Harrison, H. Sauthoff, S. Heitner, J. Jagirdar, W. N. Rom and J. G. Hay, Wild-type adenovirus decreases tumor xenograft growth, but despite viral persistence complete tumor responses are rarely achieved-deletion of the viral E1b-19-kD gene increases the viral oncolytic effect, Hum. Gene. Ther., 12 (2001), 1323-1332. doi: 10.1089/104303401750270977.
[17]	P. J. Kelly, C. Daumas-Duport, D. B. Kispert, B. A. Kall, B. W. Scheithaurer and J. J. Illig, Imaging-based sterotaxic serial biopsies in untreated intracranial glial neoplasms, J. Neurosurg., 66 (1987), 865-874. doi: 10.3171/jns.1987.66.6.0865.
[18]	R. M. Lorence, A. L. Pecora, P. P. Major, S. J. Hotte, S. A. Laurie, M. S. Roberts, W. S. Groene and M. K. Bamat, Overview of phase I studies of intravenous administration of PV701, an oncolytic virus, Curr. Opin. Mol. Ther., 5 (2003), 618-624.
[19]	D. Makower, A. Rozenblit, H. Kaufman, M. Edelman, M. E. Lane, J. Zwiebel, H. Haynes and S. Wadler, Phase II clinical trial of intralesional administration of the oncolytic adenovirus ONYX-015 in patients with hepatobiliary tumors with correlative p53 studies, Clin. Cancer Res., 9 (2003), 693-702.
[20]	E. Mandonnet, J. Y. Delattre, M. L. Tanguy, K. R. Swanson, A. F. Carpentier, H. Duffau, P. Cornu, R. Van Effenterre, E. C. Alvord, Jr. and L. Capelle, Continuous growth of mean tumor diameter in a subset of grade II gliomas, Ann. Neurol., 53 (2003), 524-528.
[21]	J. D. Murray, "Mathematical Biology II. Spatial Models and Biological Applications," 3rd edition, Springer-Verlag, New York, 2003.
[22]	A. S. Novozhilov, F. S. Berezovskaya, E. V. Koonin and G. P. Karev, Mathematical modeling of tumor therapy with oncolytic viruses: Regimes with complete tumor elimination within the framework of deterministic models, Biology Direct, 1 (2006), 1-18.
[23]	G. Paganelli, M. Bartolomei, C. Grana, M. Ferrari, P. Rocca and M. Chinol, Radioimmunotherapy of brain tumor, Neurol. Res., 28 (2006), 518-522.
[24]	J. Pallud, E. Mandonnet, H. Duffau, M. Kujas, R. Guillevin, D. Galanaud, L. Taillandier and L. Capelle, Prognostic value of initial magnetic resonance imaging growth rates for World Health Organization grade II gliomas, Ann. Neurol., 60 (2006), 380-383.
[25]	J. Peiffer, P. Kleihues and H. J. Scherer, Hans-Joachim Scherer (1906-1945), Pioneer in glioma research, Brain Pathol., 9 (1999), 241-245.
[26]	R. Rockne, J. K. Rockhill, M. Mrugala M, A. M. Spence, I. Kalet, K. Hendrickson, A. Lai, T. Cloughesy, E. C. Alvord and K. R. Swanson, Predicting the efficacy of radiotherapy in individual glioblastoma patients in vivo: A mathematical modeling approach, Phys. Med. Biol., 55 (2010), 3271-3285.
[27]	D. C. Shrieve, E. Alexander III, P. Y. Wen, H. M. Kooy, P. M. Blackand and J. S. Loeffler, Comparison of sterotactic radiosurgery and brachytherapy in the treatment of recurrent glioblastoma multiforme, Neurosurgery, 36 (1995), 275-282.
[28]	D. L. Silbergeld and M. R. Chicoine, Isolation and characterization of human malignant glioma cells from histologically normal brain, J. Neurosurg., 86 (1997), 525-531.
[29]	K. R. Swanson, C. Bridge, J. D. Murray and E. C. Alvord Jr., Virtual and real brain tumors: Using mathematical modeling to quantify glioma growth and invasion, J. Neurolog. Sci., 216 (2003), 1-10.
[30]	K. R. Swanson, R. C. Rostomily and E. C. Alvord Jr., A mathematical modeling tool for predicting the survival of individual patients following resection of glioblastoma: A proof of principle, Br. J. Cancer, 98 (2008), 113-119.
[31]	T. Takayanagi and A. Ohuchi, A Mathematical analysis of the interactions between immunogenic cells and cytotoxic T Lymphocytes, Microbiol. Immunol., 45 (2001), 709-715.
[32]	Y. Tao and Q. Guo, A mathematical model of combined therapies against cancer using viruses and inhibitors, Science in China Series A: Mathematics, 51 (2008), 2315-2329. doi: 10.1007/s11425-008-0070-7.
[33]	L. Wang and M. Y. Li, Diffusion-driven instability in reaction-diffusion systems, J. Math. Analysis and Applications, 254 (2001), 138-153. doi: 10.1006/jmaa.2000.7220.
[34]	D. Wodarz and N. Komarova, "Computational Biology of Cancer: Lecture Notes and Mathematical Modeling," World Scientific Publishing Company, Singapore, 2005.
[35]	D. Wodarz, Viruses as antitumor weapons: Defining conditions for tumor remission, Cancer Res., 61 (2001), 3501-3507.
[36]	D. Wodarz and N. Komarova, Towards predictive computational models of oncolytic virus therapy: basis for experimental validation and model selection, PLoS ONE, 4 (2009), e4271. doi: 10.1371/journal.pone.0004271.
[37]	J. T. Wu, H. M. Byrne, D. H. Kirn and L. M. Wein, Modeling and analysis of a virus that replicates selectively in tumor cells, Bull. Math. Biol., 63 (2001), 731-768.
[38]	J. T. Wu, D. H. Kirn and L. M. Wein, Analysis of a three-way race between tumor growth, a replication- competent virus and an immune response, Bull. Math. Biol., 66 (2004), 605-625. doi: 10.1016/j.bulm.2003.08.016.
[39]	R. Zurakowskia and D. Wodarz, Model-driven approaches for in vitro combination therapy using ONYX-015 replicating oncolytic adenovirus, J. Theor. Biol., 245 (2007), 1-8. doi: 10.1016/j.jtbi.2006.09.029.

show all references

References:

[1]	E. C. Alvord Jr and C. M. Shaw, Neoplasms affecting the nervous system of the elderly, in "The Pathology of the Aging Human Nervous System" (ed. S. Duckett), Lea and Fabiger, Philadelphia, (1991), 210-286.
[2]	D. D. Barker and A. J. Berk, Adenovirus proteins from both E1B reading frames are required for transformation of rodent cells by viral infection and DNA transfection, Virology, 156 (1987), 107-121. doi: 10.1016/0042-6822(87)90441-7.
[3]	N. Bagheri, M. Shiina, D. A. Lauffenburger and W. M. Korn, A dynamical systems model for combinatorial cancer therapy enhances oncolytic adenovirus efficacy by MEK-Inhibition, PLoS Comput. Biol., 7 (2011), e1001085. doi: 10.1371/journal.pcbi.1001085.
[4]	F. G. Blankenberg, R. L. Teplitz, W. Ellis, M. S. Salamat, B. H. Min, L. Hall, D. B. Boothroyd, I. M. Johnstone and D. R. Enzmann, The influence of volumetric tumor doubling time, DNA ploidy, and histologic grade on the survival of patients with intracranial astrocytomas, AJNR Am. J. Neuroradiol, 16 (1995), 1001-1012.
[5]	P. C. Burger, E. R. Heinz, T. Shibata and P. Kleihues, Topographic anatomy and CT correlations in the untreated glioblastoma multiforme, J. Neurosurg, 68 (1988), 698-704. doi: 10.3171/jns.1988.68.5.0698.
[6]	B. I. Camara and H. Mokrani, Analysis of wave solutions of an adhenovirus-tumor cell system, Abstract and Applied Analysis, (ID 590326), (2012), 1-13. doi: 10.1155/2012/590326.
[7]	G. Cherubini, T. Petouchoff, M. Grossi, S. Piersanti, E. Cundari and I. Saggio, E1B55K-deleted adenovirus (ONYX-015) overrides G1/S and G2/M checkpoints and causes mitotic catastrophe and endoreduplication in p53-proficient normal cells, Cell Cycle, 5 (2006), 2244-2252.
[8]	An. Claes, A. J. Idema and P. Wesseling, Diffuse glioma growth: A guerilla war, Acta Neuropathol, 114 (2007), 443-458. doi: 10.1007/s00401-007-0293-7.
[9]	J. C. Concannon, S. Kramer S and R. Berry, The extent of intracranial gliomata at autopsy and its relation to techniques used in radiation therapy of brain tumors, Am. J. Roentgenol. Radium Ther. Nucl. Med., 84 (1960), 99-107.
[10]	L. K. Csatary, G. Gosztonyi, J. Szeberenyi, Z. Fabian, V. Liszka, B. Bodey and C. M. Csatary, MTH-68/H oncolytic viral treatment in human high-grade gliomas, J. Neurooncol, 67 (2004), 83-93. doi: 10.1023/B:NEON.0000021735.85511.05.
[11]	K. J. Excoffon, G. L. Traver and J. Zabner, The role of the extracellular domain in the biology of the coxsackievirus and adenovirus receptor, Am. J. Respir. Cell Mol. Biol., 32 (2005), 498-503. doi: 10.1165/rcmb.2005-0031OC.
[12]	E. Fan, Extended tanh-function method and its applications to nonlinear equations, Phys. Lett. A, 277 (2000), 212-218. doi: 10.1016/S0375-9601(00)00725-8.
[13]	A. Friedman and Y. Tao, Analysis of a model of a virus that replicates selectively in tumor cells, J. Math. Biol., 47 (2003), 391-423. doi: 10.1007/s00285-003-0199-5.
[14]	X. Ge and M. Arcak, A new sufficient condition for additive D-stability and application to cyclic reaction-diffusion models, American Control Conference, (2009), 2904-2909. doi: 10.1109/ACC.2009.5160022.
[15]	H. L. Harpold, E. C. Alvord Jr. and K. R. Swanson, The evolution of mathematical modeling of glioma proliferation and invasion, J. Neuropathol. Exp. Neurol., 66 (2007), 1-9. doi: 10.1097/nen.0b013e31802d9000.
[16]	D. Harrison, H. Sauthoff, S. Heitner, J. Jagirdar, W. N. Rom and J. G. Hay, Wild-type adenovirus decreases tumor xenograft growth, but despite viral persistence complete tumor responses are rarely achieved-deletion of the viral E1b-19-kD gene increases the viral oncolytic effect, Hum. Gene. Ther., 12 (2001), 1323-1332. doi: 10.1089/104303401750270977.
[17]	P. J. Kelly, C. Daumas-Duport, D. B. Kispert, B. A. Kall, B. W. Scheithaurer and J. J. Illig, Imaging-based sterotaxic serial biopsies in untreated intracranial glial neoplasms, J. Neurosurg., 66 (1987), 865-874. doi: 10.3171/jns.1987.66.6.0865.
[18]	R. M. Lorence, A. L. Pecora, P. P. Major, S. J. Hotte, S. A. Laurie, M. S. Roberts, W. S. Groene and M. K. Bamat, Overview of phase I studies of intravenous administration of PV701, an oncolytic virus, Curr. Opin. Mol. Ther., 5 (2003), 618-624.
[19]	D. Makower, A. Rozenblit, H. Kaufman, M. Edelman, M. E. Lane, J. Zwiebel, H. Haynes and S. Wadler, Phase II clinical trial of intralesional administration of the oncolytic adenovirus ONYX-015 in patients with hepatobiliary tumors with correlative p53 studies, Clin. Cancer Res., 9 (2003), 693-702.
[20]	E. Mandonnet, J. Y. Delattre, M. L. Tanguy, K. R. Swanson, A. F. Carpentier, H. Duffau, P. Cornu, R. Van Effenterre, E. C. Alvord, Jr. and L. Capelle, Continuous growth of mean tumor diameter in a subset of grade II gliomas, Ann. Neurol., 53 (2003), 524-528.
[21]	J. D. Murray, "Mathematical Biology II. Spatial Models and Biological Applications," 3rd edition, Springer-Verlag, New York, 2003.
[22]	A. S. Novozhilov, F. S. Berezovskaya, E. V. Koonin and G. P. Karev, Mathematical modeling of tumor therapy with oncolytic viruses: Regimes with complete tumor elimination within the framework of deterministic models, Biology Direct, 1 (2006), 1-18.
[23]	G. Paganelli, M. Bartolomei, C. Grana, M. Ferrari, P. Rocca and M. Chinol, Radioimmunotherapy of brain tumor, Neurol. Res., 28 (2006), 518-522.
[24]	J. Pallud, E. Mandonnet, H. Duffau, M. Kujas, R. Guillevin, D. Galanaud, L. Taillandier and L. Capelle, Prognostic value of initial magnetic resonance imaging growth rates for World Health Organization grade II gliomas, Ann. Neurol., 60 (2006), 380-383.
[25]	J. Peiffer, P. Kleihues and H. J. Scherer, Hans-Joachim Scherer (1906-1945), Pioneer in glioma research, Brain Pathol., 9 (1999), 241-245.
[26]	R. Rockne, J. K. Rockhill, M. Mrugala M, A. M. Spence, I. Kalet, K. Hendrickson, A. Lai, T. Cloughesy, E. C. Alvord and K. R. Swanson, Predicting the efficacy of radiotherapy in individual glioblastoma patients in vivo: A mathematical modeling approach, Phys. Med. Biol., 55 (2010), 3271-3285.
[27]	D. C. Shrieve, E. Alexander III, P. Y. Wen, H. M. Kooy, P. M. Blackand and J. S. Loeffler, Comparison of sterotactic radiosurgery and brachytherapy in the treatment of recurrent glioblastoma multiforme, Neurosurgery, 36 (1995), 275-282.
[28]	D. L. Silbergeld and M. R. Chicoine, Isolation and characterization of human malignant glioma cells from histologically normal brain, J. Neurosurg., 86 (1997), 525-531.
[29]	K. R. Swanson, C. Bridge, J. D. Murray and E. C. Alvord Jr., Virtual and real brain tumors: Using mathematical modeling to quantify glioma growth and invasion, J. Neurolog. Sci., 216 (2003), 1-10.
[30]	K. R. Swanson, R. C. Rostomily and E. C. Alvord Jr., A mathematical modeling tool for predicting the survival of individual patients following resection of glioblastoma: A proof of principle, Br. J. Cancer, 98 (2008), 113-119.
[31]	T. Takayanagi and A. Ohuchi, A Mathematical analysis of the interactions between immunogenic cells and cytotoxic T Lymphocytes, Microbiol. Immunol., 45 (2001), 709-715.
[32]	Y. Tao and Q. Guo, A mathematical model of combined therapies against cancer using viruses and inhibitors, Science in China Series A: Mathematics, 51 (2008), 2315-2329. doi: 10.1007/s11425-008-0070-7.
[33]	L. Wang and M. Y. Li, Diffusion-driven instability in reaction-diffusion systems, J. Math. Analysis and Applications, 254 (2001), 138-153. doi: 10.1006/jmaa.2000.7220.
[34]	D. Wodarz and N. Komarova, "Computational Biology of Cancer: Lecture Notes and Mathematical Modeling," World Scientific Publishing Company, Singapore, 2005.
[35]	D. Wodarz, Viruses as antitumor weapons: Defining conditions for tumor remission, Cancer Res., 61 (2001), 3501-3507.
[36]	D. Wodarz and N. Komarova, Towards predictive computational models of oncolytic virus therapy: basis for experimental validation and model selection, PLoS ONE, 4 (2009), e4271. doi: 10.1371/journal.pone.0004271.
[37]	J. T. Wu, H. M. Byrne, D. H. Kirn and L. M. Wein, Modeling and analysis of a virus that replicates selectively in tumor cells, Bull. Math. Biol., 63 (2001), 731-768.
[38]	J. T. Wu, D. H. Kirn and L. M. Wein, Analysis of a three-way race between tumor growth, a replication- competent virus and an immune response, Bull. Math. Biol., 66 (2004), 605-625. doi: 10.1016/j.bulm.2003.08.016.
[39]	R. Zurakowskia and D. Wodarz, Model-driven approaches for in vitro combination therapy using ONYX-015 replicating oncolytic adenovirus, J. Theor. Biol., 245 (2007), 1-8. doi: 10.1016/j.jtbi.2006.09.029.

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