American Institute of Mathematical Sciences

Advanced
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?

Avner Friedman 1, and  Edward M. Lungu 2,

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.
Keywords: cytokines., Pathogenesis, adaptive immune response, innate immune response.
Mathematics Subject Classification: 92D3.
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 (Suppl) (1989), S59-S79. doi: 10.1017/S0031182000083426.  Google Scholar

[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), 229-266. doi: 10.1051/mmnp:2008051.  Google Scholar

[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), 2956-2963. Google Scholar

[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), 145-152. Google Scholar

[5]

R. V. Culshaw and S. Ruan, A delay-differential equation model of HIV infection of CD4$^+$ T cells, Mathematical Biosciences, 165 (2000), 27-39. doi: 10.1016/S0025-5564(00)00006-7.  Google Scholar

[6]

J. Day, A. Friedman and L. Schlesinger, Modeling the immune rheostat of macrophages in the lung in response to infection, PNAS, 106 (2009), 11246-11251. Google Scholar

[7]

C. Demangel and W. J. Britton, Interaction of dendritic cells with mycobacteria: Where the action starts, Immunol. Cells Biology, 78 (2000), 318-324. doi: 10.1046/j.1440-1711.2000.00935.x.  Google Scholar

[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), 971. Google Scholar

[9]

C. R. Engwerda and M. F. Good, Interaction between malaria parasites and the host immune system, Current Opinion in Immunology, 17 (2005), 381-387. doi: 10.1016/j.coi.2005.05.010.  Google Scholar

[10]

N. Fevre et al, The course of plasmodium chabaudi infections in interferon-$\gamma$ recepto deficient mice, Parasite Immunol, 19 (1997), 375. Google Scholar

[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), 275-285. doi: 10.1016/j.exger.2007.12.004.  Google Scholar

[12]

M. B. Graveno, A. R. McLean and D. Kwiatkowski, The regulation of malaria parasitaemia: Parameter estimates for a population model, Parasitology, 110 (1995), 115-122. doi: 10.1017/S0031182000063861.  Google Scholar

[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), 227-235. doi: 10.1017/S0031182099006368.  Google Scholar

[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), 4. doi: 10.1186/1742-4682-5-4.  Google Scholar

[15]

C. Hetzel and R. M. Anderson, The within-host cellular dynamics of bloodstage malaria: Theoretical and experimental studies, Parasitology, 113 (1996), 25-38. doi: 10.1017/S0031182000066245.  Google Scholar

[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), 535. Google Scholar

[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), 44. Google Scholar

[18]

D. Kirschner, Using mathematics to understand HIV immune dynamics, Notices of the AMS, 43 (1996), 91-202.  Google Scholar

[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), 9161-9166. doi: 10.1073/pnas.0308256101.  Google Scholar

[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), 64-70. Google Scholar

[21]

N. Mideo, T. Day and A. F. Read, Modelling malaria pathogenesis, Cellular Microbiology, 10 (2008), 1947-1955. doi: 10.1111/j.1462-5822.2008.01208.x.  Google Scholar

[22]

T. Marijani, "Interaction Between the Malaria Parasite and the Host Immune System," Ph.D thesis, Stellenbosch University, RSA. 2012. Google Scholar

[23]

R. E. L. Paul and V. Robert, The evolutionary ecology of plasmodium, Ecol. Lett., 6 (2003), 866-880. doi: 10.1046/j.1461-0248.2003.00509.x.  Google Scholar

[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), 577-586. doi: 10.1016/j.meegid.2007.04.004.  Google Scholar

[25]

Roll Back Malaria, "Malaria in Africa," WHO. 2008, http://www.rollbackmalaria.org. Google Scholar

[26]

K. A. Rockett et al, Killing of Plasmodium falciparum in vitro by nitric oxide derivatives, Infect. Immun., 59 (1991), 3280-3283. Google Scholar

[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), 2545-2556. Google Scholar

[28]

H. L. Shear et al, Role of IFN-$\gamma$ in lethal and nonlethal malaria in susceptible and resistant hosts, J. Immunol., 143 (1989), 2038. Google Scholar

[29]

J. B. De Souza et al, Early $\gamma$ interferon responses in lethal and nonlethal murine blood stage malaria, Infect. Immun., 65 (1997), 1593. Google Scholar

[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), 16-24. Google Scholar

[31]

O. M. Riveo-Lezcano, Cytokine as immunomodulators in tuberclusis therapy, Resent Patents on Anti-infective Drug Discovery, 3 (2008), 168-176. Google Scholar

[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), 29-48. doi: 10.1016/S0025-5564(02)00108-6.  Google Scholar

show all references

References:
[1]

R. M. Anderson, R. M. May and S. Gupta, Non-linear phenomena in host-parasite interactions, Parasitology, 99 (Suppl) (1989), S59-S79. doi: 10.1017/S0031182000083426.  Google Scholar

[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), 229-266. doi: 10.1051/mmnp:2008051.  Google Scholar

[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), 2956-2963. Google Scholar

[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), 145-152. Google Scholar

[5]

R. V. Culshaw and S. Ruan, A delay-differential equation model of HIV infection of CD4$^+$ T cells, Mathematical Biosciences, 165 (2000), 27-39. doi: 10.1016/S0025-5564(00)00006-7.  Google Scholar

[6]

J. Day, A. Friedman and L. Schlesinger, Modeling the immune rheostat of macrophages in the lung in response to infection, PNAS, 106 (2009), 11246-11251. Google Scholar

[7]

C. Demangel and W. J. Britton, Interaction of dendritic cells with mycobacteria: Where the action starts, Immunol. Cells Biology, 78 (2000), 318-324. doi: 10.1046/j.1440-1711.2000.00935.x.  Google Scholar

[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), 971. Google Scholar

[9]

C. R. Engwerda and M. F. Good, Interaction between malaria parasites and the host immune system, Current Opinion in Immunology, 17 (2005), 381-387. doi: 10.1016/j.coi.2005.05.010.  Google Scholar

[10]

N. Fevre et al, The course of plasmodium chabaudi infections in interferon-$\gamma$ recepto deficient mice, Parasite Immunol, 19 (1997), 375. Google Scholar

[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), 275-285. doi: 10.1016/j.exger.2007.12.004.  Google Scholar

[12]

M. B. Graveno, A. R. McLean and D. Kwiatkowski, The regulation of malaria parasitaemia: Parameter estimates for a population model, Parasitology, 110 (1995), 115-122. doi: 10.1017/S0031182000063861.  Google Scholar

[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), 227-235. doi: 10.1017/S0031182099006368.  Google Scholar

[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), 4. doi: 10.1186/1742-4682-5-4.  Google Scholar

[15]

C. Hetzel and R. M. Anderson, The within-host cellular dynamics of bloodstage malaria: Theoretical and experimental studies, Parasitology, 113 (1996), 25-38. doi: 10.1017/S0031182000066245.  Google Scholar

[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), 535. Google Scholar

[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), 44. Google Scholar

[18]

D. Kirschner, Using mathematics to understand HIV immune dynamics, Notices of the AMS, 43 (1996), 91-202.  Google Scholar

[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), 9161-9166. doi: 10.1073/pnas.0308256101.  Google Scholar

[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), 64-70. Google Scholar

[21]

N. Mideo, T. Day and A. F. Read, Modelling malaria pathogenesis, Cellular Microbiology, 10 (2008), 1947-1955. doi: 10.1111/j.1462-5822.2008.01208.x.  Google Scholar

[22]

T. Marijani, "Interaction Between the Malaria Parasite and the Host Immune System," Ph.D thesis, Stellenbosch University, RSA. 2012. Google Scholar

[23]

R. E. L. Paul and V. Robert, The evolutionary ecology of plasmodium, Ecol. Lett., 6 (2003), 866-880. doi: 10.1046/j.1461-0248.2003.00509.x.  Google Scholar

[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), 577-586. doi: 10.1016/j.meegid.2007.04.004.  Google Scholar

[25]

Roll Back Malaria, "Malaria in Africa," WHO. 2008, http://www.rollbackmalaria.org. Google Scholar

[26]

K. A. Rockett et al, Killing of Plasmodium falciparum in vitro by nitric oxide derivatives, Infect. Immun., 59 (1991), 3280-3283. Google Scholar

[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), 2545-2556. Google Scholar

[28]

H. L. Shear et al, Role of IFN-$\gamma$ in lethal and nonlethal malaria in susceptible and resistant hosts, J. Immunol., 143 (1989), 2038. Google Scholar

[29]

J. B. De Souza et al, Early $\gamma$ interferon responses in lethal and nonlethal murine blood stage malaria, Infect. Immun., 65 (1997), 1593. Google Scholar

[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), 16-24. Google Scholar

[31]

O. M. Riveo-Lezcano, Cytokine as immunomodulators in tuberclusis therapy, Resent Patents on Anti-infective Drug Discovery, 3 (2008), 168-176. Google Scholar

[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), 29-48. doi: 10.1016/S0025-5564(02)00108-6.  Google Scholar

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