2013, 10(3): 609-624. doi: 10.3934/mbe.2013.10.609

Can malaria parasite pathogenesis be prevented by treatment with tumor necrosis factor-alpha?

1. 

MBI, Ohio State University, Columbus, OH 43210, United States

2. 

Department of Mathematics, University of Botswana, Gaborone

Received  July 2012 Revised  November 2012 Published  April 2013

We consider a model incorporating the influence of innate and adaptive immune responses on malaria pathogenesis. By calculating the model reproduction number for a special representation of cytokine interaction, we have shown that the cytokine tumour necrosis factor-$\alpha$ can be administered to inhibit malaria infection. We have also found that if the cytokine $F^*$ and a generic drug of efficacy $\epsilon$ are administered as dual therapy then clearance of the parasite can be achieved even for a generic drug of low efficacy. Our study is recommending administration of dual therapy as a strategy to prevent parasites from developing resistance to malaria treatment drugs.
Citation: Avner Friedman, Edward M. Lungu. Can malaria parasite pathogenesis be prevented by treatment with tumor necrosis factor-alpha?. Mathematical Biosciences & Engineering, 2013, 10 (3) : 609-624. doi: 10.3934/mbe.2013.10.609
References:
[1]

R. M. Anderson, R. M. May and S. Gupta, Non-linear phenomena in host-parasite interactions,, Parasitology, 99 (1989). doi: 10.1017/S0031182000083426.

[2]

A. L. Bauer, Ian B. Hogue, Simeone Marino and Denise E. Kirschner, The effects of HIV-1 infection on latent tuberculosis,, Math. Model. Nat. Pheno, 3 (2008), 229. doi: 10.1051/mmnp:2008051.

[3]

K. Artavanis-Tsakonas and E. M. Riley, Innate immune response to malaria: Rapid induction of INF-$\gamma$ from human NK cells in live Plasmodium falciparum infected erythrocytes,, 169 (2002), 169 (2002), 2956.

[4]

K. Artavanis-Tsakonas, J. E. Tonren and E. M. Riley, The war between the malaria parasite and the immune system: Immunity, immunoregulation and immunopathology,, Clinical and Experimental Immunology, 133 (2003), 145.

[5]

R. V. Culshaw and S. Ruan, A delay-differential equation model of HIV infection of CD4$^+$ T cells,, Mathematical Biosciences, 165 (2000), 27. doi: 10.1016/S0025-5564(00)00006-7.

[6]

J. Day, A. Friedman and L. Schlesinger, Modeling the immune rheostat of macrophages in the lung in response to infection,, PNAS, 106 (2009), 11246.

[7]

C. Demangel and W. J. Britton, Interaction of dendritic cells with mycobacteria: Where the action starts,, Immunol. Cells Biology, 78 (2000), 318. doi: 10.1046/j.1440-1711.2000.00935.x.

[8]

D. Dodoo et al, Absolute levels and ratios of pro-inflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to P. falciparum malaria,, J. Infect. Dis, 185 (2002).

[9]

C. R. Engwerda and M. F. Good, Interaction between malaria parasites and the host immune system,, Current Opinion in Immunology, 17 (2005), 381. doi: 10.1016/j.coi.2005.05.010.

[10]

N. Fevre et al, The course of plasmodium chabaudi infections in interferon-$\gamma$ recepto deficient mice,, Parasite Immunol, 19 (1997).

[11]

A. Friedman, J. Turner and B. Szamolay, A model on the influence of age on immunity to infection with mycobacterium tuberculosis,, Eeperimental Gerontology, 43 (2008), 275. doi: 10.1016/j.exger.2007.12.004.

[12]

M. B. Graveno, A. R. McLean and D. Kwiatkowski, The regulation of malaria parasitaemia: Parameter estimates for a population model,, Parasitology, 110 (1995), 115. doi: 10.1017/S0031182000063861.

[13]

B. M. Hoshem, R. Heinrich, W. D. Stein and H. Ginsburg, Mathematical modelling of the within-host dynamics of plasmodium falciparum,, Parasitology, 121 (2000), 227. doi: 10.1017/S0031182099006368.

[14]

A. Hoare, D. G. Regan and D. P. Wilson, Sampling and sensitivity analysis tools and SASAT for computational modeling,, Journal of Theoretical Biology and Medical Modeling, 5 (2008). doi: 10.1186/1742-4682-5-4.

[15]

C. Hetzel and R. M. Anderson, The within-host cellular dynamics of bloodstage malaria: Theoretical and experimental studies,, Parasitology, 113 (1996), 25. doi: 10.1017/S0031182000066245.

[16]

P. Jacob et al, Th1-associated increase in tumor necrosis factor $\alpha$ expression in the spleen correlates with resistance to blood-stage malaria in mice,, Infect. Immun, 64 (1996).

[17]

P. Jacob et al, In vivo regulation of nitric oxide production by tumor necrosis factor $\alpha$ and $\gamma$ interferon, but not by interferon leukin-4, during blood stage malaria in mice,, Infect. Immun, 64 (1996).

[18]

D. Kirschner, Using mathematics to understand HIV immune dynamics,, Notices of the AMS, 43 (1996), 91.

[19]

P. G McQueen and F. E. McKenzie, Age-structured red blood cell susceptibility and the dynamics of malaria infections,, Proc. Natl. Acad. Sci. USA, 101 (2004), 9161. doi: 10.1073/pnas.0308256101.

[20]

V. Mung'Ala-Odera et al, The burden of the neurocognitive impairment associated with Plasmodium falciparum malaria in sub-sahara Africa,, Am. J. Trop. Med. Hyg., 71 (2004), 64.

[21]

N. Mideo, T. Day and A. F. Read, Modelling malaria pathogenesis,, Cellular Microbiology, 10 (2008), 1947. doi: 10.1111/j.1462-5822.2008.01208.x.

[22]

T. Marijani, "Interaction Between the Malaria Parasite and the Host Immune System,", Ph.D thesis, (2012).

[23]

R. E. L. Paul and V. Robert, The evolutionary ecology of plasmodium,, Ecol. Lett., 6 (2003), 866. doi: 10.1046/j.1461-0248.2003.00509.x.

[24]

R. E. L. Paul, S. Bonnet, C. Boudin, T. Tchuinkam and V. Robert, Aggregation in malaria parasites places limits on mosquito infection rates,, Infect. Genet. Evol., 7 (2007), 577. doi: 10.1016/j.meegid.2007.04.004.

[25]

Roll Back Malaria, "Malaria in Africa,", WHO. 2008, (2008).

[26]

K. A. Rockett et al, Killing of Plasmodium falciparum in vitro by nitric oxide derivatives,, Infect. Immun., 59 (1991), 3280.

[27]

M. M. Stevenson et al, IL-12-induced protection against blood-stage plasmodium chabaudi AS requires IFN-$\gamma$ and TNF-$\alpha$ and occurs via a nitric oxide-dependent mechanism,, The Journal of Immunology, 155 (1995), 2545.

[28]

H. L. Shear et al, Role of IFN-$\gamma$ in lethal and nonlethal malaria in susceptible and resistant hosts,, J. Immunol., 143 (1989).

[29]

J. B. De Souza et al, Early $\gamma$ interferon responses in lethal and nonlethal murine blood stage malaria,, Infect. Immun., 65 (1997).

[30]

R. W. Snow et al, Pediatric mortality in Africa: Plasmodium falciparum malaria as a cause or risk?,, Am. J. Trop. Med. Hyg., 71 (2004), 16.

[31]

O. M. Riveo-Lezcano, Cytokine as immunomodulators in tuberclusis therapy,, Resent Patents on Anti-infective Drug Discovery, 3 (2008), 168.

[32]

P. van den Driessche and J. Watmough, Reproduction numbers and sub-threshold endemic equilibria for compartmental models of disease transmission,, Mathematical Bioscinces, 180 (2002), 29. doi: 10.1016/S0025-5564(02)00108-6.

show all references

References:
[1]

R. M. Anderson, R. M. May and S. Gupta, Non-linear phenomena in host-parasite interactions,, Parasitology, 99 (1989). doi: 10.1017/S0031182000083426.

[2]

A. L. Bauer, Ian B. Hogue, Simeone Marino and Denise E. Kirschner, The effects of HIV-1 infection on latent tuberculosis,, Math. Model. Nat. Pheno, 3 (2008), 229. doi: 10.1051/mmnp:2008051.

[3]

K. Artavanis-Tsakonas and E. M. Riley, Innate immune response to malaria: Rapid induction of INF-$\gamma$ from human NK cells in live Plasmodium falciparum infected erythrocytes,, 169 (2002), 169 (2002), 2956.

[4]

K. Artavanis-Tsakonas, J. E. Tonren and E. M. Riley, The war between the malaria parasite and the immune system: Immunity, immunoregulation and immunopathology,, Clinical and Experimental Immunology, 133 (2003), 145.

[5]

R. V. Culshaw and S. Ruan, A delay-differential equation model of HIV infection of CD4$^+$ T cells,, Mathematical Biosciences, 165 (2000), 27. doi: 10.1016/S0025-5564(00)00006-7.

[6]

J. Day, A. Friedman and L. Schlesinger, Modeling the immune rheostat of macrophages in the lung in response to infection,, PNAS, 106 (2009), 11246.

[7]

C. Demangel and W. J. Britton, Interaction of dendritic cells with mycobacteria: Where the action starts,, Immunol. Cells Biology, 78 (2000), 318. doi: 10.1046/j.1440-1711.2000.00935.x.

[8]

D. Dodoo et al, Absolute levels and ratios of pro-inflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to P. falciparum malaria,, J. Infect. Dis, 185 (2002).

[9]

C. R. Engwerda and M. F. Good, Interaction between malaria parasites and the host immune system,, Current Opinion in Immunology, 17 (2005), 381. doi: 10.1016/j.coi.2005.05.010.

[10]

N. Fevre et al, The course of plasmodium chabaudi infections in interferon-$\gamma$ recepto deficient mice,, Parasite Immunol, 19 (1997).

[11]

A. Friedman, J. Turner and B. Szamolay, A model on the influence of age on immunity to infection with mycobacterium tuberculosis,, Eeperimental Gerontology, 43 (2008), 275. doi: 10.1016/j.exger.2007.12.004.

[12]

M. B. Graveno, A. R. McLean and D. Kwiatkowski, The regulation of malaria parasitaemia: Parameter estimates for a population model,, Parasitology, 110 (1995), 115. doi: 10.1017/S0031182000063861.

[13]

B. M. Hoshem, R. Heinrich, W. D. Stein and H. Ginsburg, Mathematical modelling of the within-host dynamics of plasmodium falciparum,, Parasitology, 121 (2000), 227. doi: 10.1017/S0031182099006368.

[14]

A. Hoare, D. G. Regan and D. P. Wilson, Sampling and sensitivity analysis tools and SASAT for computational modeling,, Journal of Theoretical Biology and Medical Modeling, 5 (2008). doi: 10.1186/1742-4682-5-4.

[15]

C. Hetzel and R. M. Anderson, The within-host cellular dynamics of bloodstage malaria: Theoretical and experimental studies,, Parasitology, 113 (1996), 25. doi: 10.1017/S0031182000066245.

[16]

P. Jacob et al, Th1-associated increase in tumor necrosis factor $\alpha$ expression in the spleen correlates with resistance to blood-stage malaria in mice,, Infect. Immun, 64 (1996).

[17]

P. Jacob et al, In vivo regulation of nitric oxide production by tumor necrosis factor $\alpha$ and $\gamma$ interferon, but not by interferon leukin-4, during blood stage malaria in mice,, Infect. Immun, 64 (1996).

[18]

D. Kirschner, Using mathematics to understand HIV immune dynamics,, Notices of the AMS, 43 (1996), 91.

[19]

P. G McQueen and F. E. McKenzie, Age-structured red blood cell susceptibility and the dynamics of malaria infections,, Proc. Natl. Acad. Sci. USA, 101 (2004), 9161. doi: 10.1073/pnas.0308256101.

[20]

V. Mung'Ala-Odera et al, The burden of the neurocognitive impairment associated with Plasmodium falciparum malaria in sub-sahara Africa,, Am. J. Trop. Med. Hyg., 71 (2004), 64.

[21]

N. Mideo, T. Day and A. F. Read, Modelling malaria pathogenesis,, Cellular Microbiology, 10 (2008), 1947. doi: 10.1111/j.1462-5822.2008.01208.x.

[22]

T. Marijani, "Interaction Between the Malaria Parasite and the Host Immune System,", Ph.D thesis, (2012).

[23]

R. E. L. Paul and V. Robert, The evolutionary ecology of plasmodium,, Ecol. Lett., 6 (2003), 866. doi: 10.1046/j.1461-0248.2003.00509.x.

[24]

R. E. L. Paul, S. Bonnet, C. Boudin, T. Tchuinkam and V. Robert, Aggregation in malaria parasites places limits on mosquito infection rates,, Infect. Genet. Evol., 7 (2007), 577. doi: 10.1016/j.meegid.2007.04.004.

[25]

Roll Back Malaria, "Malaria in Africa,", WHO. 2008, (2008).

[26]

K. A. Rockett et al, Killing of Plasmodium falciparum in vitro by nitric oxide derivatives,, Infect. Immun., 59 (1991), 3280.

[27]

M. M. Stevenson et al, IL-12-induced protection against blood-stage plasmodium chabaudi AS requires IFN-$\gamma$ and TNF-$\alpha$ and occurs via a nitric oxide-dependent mechanism,, The Journal of Immunology, 155 (1995), 2545.

[28]

H. L. Shear et al, Role of IFN-$\gamma$ in lethal and nonlethal malaria in susceptible and resistant hosts,, J. Immunol., 143 (1989).

[29]

J. B. De Souza et al, Early $\gamma$ interferon responses in lethal and nonlethal murine blood stage malaria,, Infect. Immun., 65 (1997).

[30]

R. W. Snow et al, Pediatric mortality in Africa: Plasmodium falciparum malaria as a cause or risk?,, Am. J. Trop. Med. Hyg., 71 (2004), 16.

[31]

O. M. Riveo-Lezcano, Cytokine as immunomodulators in tuberclusis therapy,, Resent Patents on Anti-infective Drug Discovery, 3 (2008), 168.

[32]

P. van den Driessche and J. Watmough, Reproduction numbers and sub-threshold endemic equilibria for compartmental models of disease transmission,, Mathematical Bioscinces, 180 (2002), 29. doi: 10.1016/S0025-5564(02)00108-6.

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