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The Evolution of Tuberculosis Virulence

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Abstract

The evolution of Mycobacterium tuberculosis presents several challenges for public health. HIV and resistance to antimycobacterial medications have evolutionary implications for how Mycobacterium tuberculosis will evolve, as these factors influence the host environment and transmission dynamics of tuberculosis strains. We present an evolutionary invasion analysis of tuberculosis that characterizes the direction of tuberculosis evolution in the context of different natural and human-driven selective pressures, including changes in tuberculosis treatment and HIV prevalence. We find that the evolution of tuberculosis virulence can be affected by treatment success rates, the relative transmissibility of emerging strains, the rate of reactivation from latency among hosts, and the life expectancy of hosts. We find that the virulence of tuberculosis strains may also increase as a consequence of rising HIV prevalence, requiring faster case detection strategies in areas where the epidemics of HIV and tuberculosis collide.

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References

  • Anderson, R.M., May, R.M., 1991. Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, London.

    Google Scholar 

  • Basu, S., , 2007. Prevention of nosocomial transmission of extensively drug-resistant tuberculosis in rural South African district hospitals: an epidemiological modelling study. Lancet 370(9597), 1500–1507.

    Article  Google Scholar 

  • Blower, S.M., Chou, T., 2004. Modeling the emergence of the ‘hot zones’: tuberculosis and the amplification dynamics of drug resistance. Nat. Med. 10(10), 1111–1116.

    Article  Google Scholar 

  • Blower, S.M., Gerberding, J.L., 1998. Understanding, predicting and controlling the emergence of drug-resistant tuberculosis: a theoretical framework. J. Mol. Med. 76(9), 624–636.

    Article  Google Scholar 

  • Blower, S.M., , 1995. The intrinsic transmission dynamics of tuberculosis epidemics. Nat. Med. 1(8), 815–821.

    Article  Google Scholar 

  • Boots, M., Sasaki, A., 1999. ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proc. Biol. Sci. 266, 1933–1938.

    Article  Google Scholar 

  • Bremerman, H.J., Thieme, H.R., 1989. A competitive-exclusion principle for pathogen virulence. J. Math. Biol. 27, 179–190.

    MathSciNet  Google Scholar 

  • Castro, K.G., Dooley, S.W., 1993. Mycobacterium tuberculosis transmission in healthcare settings: is it influenced by coinfection with human immunodeficiency virus? Infect. Control. Hosp. Epidemiol. 14(2), 65–66.

    Article  Google Scholar 

  • Cohen, T., Murray, M., 2004. Modeling epidemics of multidrug-resistant M. tuberculosis of heterogeneous fitness. Nat. Med. 10(10), 1117–1121.

    Article  Google Scholar 

  • Cohen, T. et al., 2006. Exogenous re-infection and the dynamics of tuberculosis epidemics: local effects in a network model of transmission. J. R. Soc. Interface.

  • Corbett, E.L., , 2006. Tuberculosis in sub-Saharan Africa: opportunities, challenges, and change in the era of antiretroviral treatment. Lancet 367(9514), 926–937.

    Article  Google Scholar 

  • Crofton, J., Horne, N., Miller, F., 1999. Pulmonary tuberculosis in adults. In: Clinical Tuberculosis. MacMillan, London.

    Google Scholar 

  • Cruciani, M., , 2001. The impact of human immunodeficiency virus type 1 on infectiousness of tuberculosis: a meta-analysis. Clin. Infect. Dis. 33(11), 1922–1930.

    Article  Google Scholar 

  • Daley, C.L., , 1992. An outbreak of tuberculosis with accelerated progression among persons infected with the human immunodeficiency virus. An analysis using restriction-fragment-length polymorphisms. N. Engl. J. Med. 326(4), 231–235.

    MathSciNet  Google Scholar 

  • Di Perri, G., , 1989. Nosocomial epidemic of active tuberculosis among HIV-infected patients. Lancet 2(8678–8679), 1502–1504.

    Google Scholar 

  • Dye, C., Espinal, M.A., 2001. Will tuberculosis become resistant to all antibiotics? Proc. Biol. Sci. 268(1462), 45–52.

    Article  Google Scholar 

  • Dye, C., Williams, B.G., 2000. Criteria for the control of drug-resistant tuberculosis. Proc. Natl. Acad. Sci. USA 97(14), 8180–8185.

    Article  Google Scholar 

  • Dye, C., , 1998. Prospects for worldwide tuberculosis control under the WHO DOTS strategy. Directly observed short-course therapy. Lancet 352(9144), 1886–1891.

    Article  Google Scholar 

  • Dye, C., , 2002. Erasing the world’s slow stain: strategies to beat multidrug-resistant tuberculosis. Science 295(5562), 2042–2046.

    Article  Google Scholar 

  • Ebert, D., Bull, J.J., 2003. Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends Microbiol. 11(1), 15–20.

    Article  Google Scholar 

  • ECA, 2006. Beijing/W genotype mycobacterium tuberculosis and drug resistance. Emerg. Infect. Dis. 12(5), 736–743.

    Google Scholar 

  • Edlin, B.R., , 1992. An outbreak of multidrug-resistant tuberculosis among hospitalized patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 326(23), 1514–1521.

    Article  Google Scholar 

  • Ernst, J.D., Trevejo-Nunez, G., Banaiee, N., 2007. Genomics and the evolution, pathogenesis, and diagnosis of tuberculosis. J. Clin. Invest. 117(7), 1738–1745.

    Article  Google Scholar 

  • Escombe, A.R., , 2007. The detection of airborne transmission of tuberculosis from HIV-infected patients, using an in vivo air sampling model. Clin. Infect. Dis. 44(10), 1349–1357.

    Article  Google Scholar 

  • Eshel, I., 1983. Evolutionary and continuous stability. J. Theor. Biol. 103, 99–111.

    Article  MathSciNet  Google Scholar 

  • Feng, Z., Castillo-Chavez, C., Capurro, A.F., 2000. A model for tuberculosis with exogenous reinfection. Theor. Popul. Biol. 57(3), 235–247.

    Article  MATH  Google Scholar 

  • Friedland, G., 2007. Tuberculosis, drug resistance and HIV/AIDS: a triple threat. Curr. Infect. Dis. Rep. 9(3), 252–261.

    Article  MathSciNet  Google Scholar 

  • Friedland, G., Churchyard, G.J., Nardell, E., 2007. Tuberculosis and HIV coinfection: current state of knowledge and research priorities. J. Infect. Dis. 196(1), S1–S3.

    Article  Google Scholar 

  • Gandhi, N.R., , 2006. Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet 368(9547), 1575–1580.

    Article  Google Scholar 

  • Githui, W.A., , 2004. Identification of MDR-TB Beijing/W and other mycobacterium tuberculosis genotypes in Nairobi. Kenya. Int. J. Tuberc. Lung. Dis. 8(3), 352–360.

    Google Scholar 

  • Health Systems Trust, 2007. HIV Prevalence. HST, Durban.

    Google Scholar 

  • Keeler, E., , 2006. Reducing the global burden of tuberculosis: the contribution of improved diagnostics. Nature 444(1), 49–57.

    Article  MathSciNet  Google Scholar 

  • Keeling, M.J., Rohani, P., 2007. Modeling Infectious Diseases in Humans and Animals. Princeton University Press, Princeton.

    Google Scholar 

  • Lan, N.T., , 2003. Mycobacterium tuberculosis Beijing genotype and risk for treatment failure and relapse. Vietnam. Emerg. Infect. Dis. 9(12), 1633–1635.

    Google Scholar 

  • Lawn, S.D. et al., 2007. Early mortality among patients with HIV-associated TB in Africa: implications for the time to initiate ART. In: 14th Conference on Retroviruses and Opportunistic Infections, Los Angeles.

  • Levin, B.R., 1996. The evolution and maintenance of virulence in microparasites. Emerg. Infect. Dis. 2(2), 93–102.

    Google Scholar 

  • Lipsitch, M., Murray, M.B., 2003. Multiple equilibria: tuberculosis transmission require unrealistic assumptions. Theor. Popul. Biol. 63(2), 169–170.

    Article  Google Scholar 

  • Mann, N.H., , 2003. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424(6950), 741.

    Article  Google Scholar 

  • Moore, D.A., , 2006. Microscopic-observation drug-susceptibility assay for the diagnosis of TB. N. Engl. J. Med. 355(15), 1539–1550.

    Article  Google Scholar 

  • Otto, S.P., Day, T., 2007. A Biologist’s Guide to Mathematical Modeling in Ecology and Evolution. Princeton University Press, Princeton.

    MATH  Google Scholar 

  • Pillay, V., Sturm, A.W., 2007. Evolution of the extensively dRUG-resistant F15/LAM4/KZN strain of mycobacterium tuberculosis in KwaZulu-Natal, South Africa. Clin. Infect. Dis. 45(11), 1409–1414.

    Article  Google Scholar 

  • Sherman, D.R., , 1996. Compensatory ahpC gene expression in isoniazid-resistant mycobacterium tuberculosis. Science 272(5268), 1641–1643.

    Article  Google Scholar 

  • Small, P.M., , 1993. Exogenous reinfection with multidrug-resistant Mycobacterium tuberculosis in patients with advanced HIV infection. N. Engl. J. Med. 328(16), 1137–1144.

    Article  Google Scholar 

  • Smith, J.M., Price, G.R., 1973. The logic of animal conflict. Nature 246, 15–18.

    Article  Google Scholar 

  • Special Programme for Tropical Diseases Research, 2006. Diagnostics for Tuberculosis: Global Demand and Market Potential. WHO, Paris.

    Google Scholar 

  • van den Driessche, P., Watmough, J., 2002. Reproduction numbers and sub-threshold endemic equilibria for compartmental models of disease transmission. Math. Biosci. 180, 29–48.

    Article  MATH  MathSciNet  Google Scholar 

  • Williams, B.G., Dye, C., 2003. Antiretroviral drugs for tuberculosis control in the era of HIV/AIDS. Science 301(5639), 1535–1537.

    Article  Google Scholar 

  • Williams, B.G., , 2005. The impact of HIV/AIDS on the control of tuberculosis in India. Proc. Natl. Acad. Sci. USA 102(27), 9619–9624.

    Article  Google Scholar 

  • World Health Organization, 2005. The Impact of HIV on TB in Africa. WHO, Paris.

    Google Scholar 

  • World Health Organization, 2006. Progress on Global Access to HIV Antiretroviral Therapy: A Report on “3 by 5” and beyond. WHO, Paris.

    Google Scholar 

  • World Health Organization, 2007a. Global Tuberculosis Control: Surveillance, Planning, Financing. WHO, Paris.

    Google Scholar 

  • World Health Organization, 2007b. Global Tuberculosis Control—Surveillance, Planning, Financing. WHO, Paris.

    Google Scholar 

  • Wright, S., 1931. Evolution in Mendelian populations. Genetics 16, 97–159.

    Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Epidemiology and Public Health, Yale University School of Medicine, 60 College Street, New Haven, CT, 06520, USA

    Sanjay Basu & Alison P. Galvani

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  1. Sanjay Basu
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  2. Alison P. Galvani
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Correspondence to Sanjay Basu.

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Basu, S., Galvani, A.P. The Evolution of Tuberculosis Virulence. Bull. Math. Biol. 71, 1073–1088 (2009). https://doi.org/10.1007/s11538-009-9394-x

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  • DOI: https://doi.org/10.1007/s11538-009-9394-x

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