Advertisement

Modelling the HIV-Associated TB Epidemic and the Impact of Interventions Aimed at Epidemic Control

  • P. J. DoddEmail author
  • C. Pretorius
  • B. G. Williams
Chapter

Abstract

In this chapter, we focus on mathematical models of tuberculosis epidemiology (TB) that include interactions with HIV and an explicit representation of transmission. We review the natural history of TB and illustrate how its features are simplified and incorporated in mathematical models. We then review the ways HIV influences the natural history of TB, the interventions that have been considered in models, and the way these individual-level effects are represented in models. We then go on to consider population-level effects, reviewing the TB/HIV modelling literature. We first review studies whose focus was on purely epidemiological modelling, and then studies whose focus was on modelling the impact of interventions. We conclude with a summary of the uses and achievements of TB/HIV modelling and some suggested future directions.

Keywords

Tuberculosis Human immunodeficiency virus Mathematical modelling Transmission modelling TB/HIV Epidemiological modelling Economic evaluation Natural history Epidemiology 

References

  1. 1.
    Williams BG, Granich R, De Cock KM, Glaziou P, Sharma A, Dye C (2010) Antiretroviral therapy for tuberculosis control in nine African countries. Proc Natl Acad Sci U S A 107:19485–19489PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Corbett EL, Watt CJ, Walker N et al (2003) The growing burden of tuberculosis. Arch Intern Med 163:1009PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    World Health Organisation (2017) Global tuberculosis report 2017Google Scholar
  4. 4.
    Dye C, Garnett GP, Sleeman K, Williams BG (1998) Prospects for worldwide tuberculosis control under the WHO DOTS strategy. Directly observed short-course therapy. Lancet 352:1886–1891PubMedCrossRefGoogle Scholar
  5. 5.
    Dye C. The population biology of tuberculosis. 2017.Google Scholar
  6. 6.
    Menzies NA, Wolf E, Connors D, Cohen T, Hill AN, Yaesoubi R, Galer K, White PJ, Abubakar I, Salomon JA (2018) Progression from latent infection to active disease in dynamic TB transmission models: a systematic review. Lancet Infect Dis 18(8):e228–e238PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Marais BJ, Gie RP, Schaaf HS et al (2004) The natural history of childhood intra-thoracic tuberculosis: a critical review of literature from the pre-chemotherapy era. Int J Tuberc Lung Dis 8:392–402PubMedGoogle Scholar
  8. 8.
    Vynnycky E, Fine PE (1997) The natural history of tuberculosis: the implications of age-dependent risks of disease and the role of reinfection. Epidemiol Infect 119:183–201PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Comstock GW, Livesay VT, Woolpert SF (1974) The prognosis of a positive tuberculin reaction in childhood and adolescence. Am J Epidemiol 99:131–138PubMedCrossRefGoogle Scholar
  10. 10.
    Sloot R, van der Loeff MF S, Kouw PM, Borgdorff MW (2014) Risk of tuberculosis after recent exposure. A 10-year follow-up study of contacts in Amsterdam. Am J Respir Crit Care Med 190:1044–1052PubMedCrossRefGoogle Scholar
  11. 11.
    Ragonnet R, Trauer JM, Scott N, Meehan MT, Denholm JT, McBryde ES. Optimally capturing latency dynamics in models of tuberculosis transmission. Epidemics 2017.  https://doi.org/10.1016/j.epidem.2017.06.002PubMedCrossRefGoogle Scholar
  12. 12.
    Andrews JR, Noubary F, Walensky RP, Cerda R, Losina E, Horsburgh CR (2012) Risk of progression to active tuberculosis following reinfection with Mycobacterium tuberculosis. Clin Infect Dis 54:784–791PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Sutherland I, Svandova E, Radhakrishna S (1976) Alternative models for the development of tuberculosis disease following infection with tubercle bacilli. Bull Int Union Tuberc 51:171–179PubMedGoogle Scholar
  14. 14.
    Tostmann A, Kik SV, Kalisvaart NA et al (2008) Tuberculosis transmission by patients with smear-negative pulmonary tuberculosis in a large cohort in The Netherlands. Clin Infect Dis 47:1135–1142PubMedCrossRefGoogle Scholar
  15. 15.
    Hernandez-Garduno E (2004) Transmission of tuberculosis from smear negative patients: a molecular epidemiology study. Thorax 59:286–290PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Esmail H, Barry CE 3rd, Young DB, Wilkinson RJ (2014) The ongoing challenge of latent tuberculosis. Philos Trans R Soc Lond Ser B Biol Sci 369:20130437CrossRefGoogle Scholar
  17. 17.
    Onozaki I, Law I, Sismanidis C, Zignol M, Glaziou P, Floyd K (2015) National tuberculosis prevalence surveys in Asia, 1990–2012: an overview of results and lessons learned. Trop Med Int Health 20:1128–1145PubMedCrossRefGoogle Scholar
  18. 18.
    Trunz BB, Bourdin Trunz B, Fine P, Dye C (2006) Effect of BCG vaccination on childhood tuberculous meningitis and miliary tuberculosis worldwide: a meta-analysis and assessment of cost-effectiveness. Lancet 367:1173–1180PubMedCrossRefGoogle Scholar
  19. 19.
    van Leth F, van der Werf MJ, Borgdorff MW (2008) Prevalence of tuberculous infection and incidence of tuberculosis: a re-assessment of the Styblo rule. Bull World Health Organ 86:20–26PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Tiemersma EW, van der Werf MJ, Borgdorff MW, Williams BG, Nagelkerke NJD (2011) Natural history of tuberculosis: duration and fatality of untreated pulmonary tuberculosis in HIV negative patients: a systematic review. PLoS One 6:e17601PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Thompson BC (1943) Survival rates in pulmonary tuberculosis. Br Med J 2:721–721PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Jindani A, Aber VR, Edwards EA, Mitchison DA (1980) The early bactericidal activity of drugs in patients with pulmonary tuberculosis. Am Rev Respir Dis 121:939–949PubMedGoogle Scholar
  23. 23.
    Loudon RG, Spohn SK (1969) Cough frequency and infectivity in patients with pulmonary tuberculosis. Am Rev Respir Dis 99:109–111PubMedGoogle Scholar
  24. 24.
    Davies C. The eradication of tuberculosis in Rhodesia: with particular reference to the Midlands and South Eastern Provinces. 1966.Google Scholar
  25. 25.
    Marx FM, Dunbar R, Enarson DA et al (2014) The temporal dynamics of relapse and reinfection tuberculosis after successful treatment: a retrospective cohort study. Clin Infect Dis 58:1676–1683PubMedCrossRefGoogle Scholar
  26. 26.
    Marx FM, Floyd S, Ayles H, Godfrey-Faussett P, Beyers N, Cohen T (2016) High burden of prevalent tuberculosis among previously treated people in Southern Africa suggests potential for targeted control interventions. Eur Respir J 48:1227–1230PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Dodd PJ, Gardiner E, Coghlan R, Seddon JA (2014) Burden of childhood tuberculosis in 22 high-burden countries: a mathematical modelling study. Lancet Glob Health 2:e453–e459PubMedCrossRefGoogle Scholar
  28. 28.
    Dodd PJ, Sismanidis C, Seddon JA (2016) Global burden of drug-resistant tuberculosis in children: a mathematical modelling study. Lancet Infect Dis 16:1193–1201PubMedCrossRefGoogle Scholar
  29. 29.
    Horton KC, MacPherson P, Houben RMGJ, White RG, Corbett EL (2016) Sex differences in tuberculosis burden and notifications in low- and middle-income countries: a systematic review and meta-analysis. PLoS Med 13:e1002119PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Stevenson CR, Forouhi NG, Roglic G et al (2007) Diabetes and tuberculosis: the impact of the diabetes epidemic on tuberculosis incidence. BMC Public Health 7:234PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Corbett EL, Churchyard GJ, Clayton TC et al (2000) HIV infection and silicosis: the impact of two potent risk factors on the incidence of mycobacterial disease in South African miners. AIDS 14:2759–2768PubMedCrossRefGoogle Scholar
  32. 32.
    Lin H-H, Ezzati M, Murray M (2007) Tobacco smoke, indoor air pollution and tuberculosis: a systematic review and meta-analysis. PLoS Med 4:e20PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Lönnroth K, Williams BG, Cegielski P, Dye C (2010) A consistent log-linear relationship between tuberculosis incidence and body mass index. Int J Epidemiol 39:149–155PubMedCrossRefGoogle Scholar
  34. 34.
    Lönnroth K, Jaramillo E, Williams BG, Dye C, Raviglione M (2009) Drivers of tuberculosis epidemics: the role of risk factors and social determinants. Soc Sci Med 68:2240–2246PubMedCrossRefGoogle Scholar
  35. 35.
    Williams BG, Dye C (2003) Antiretroviral drugs for tuberculosis control in the era of HIV/AIDS. Science 301:1535–1537PubMedCrossRefGoogle Scholar
  36. 36.
    Ellis PK, Martin WJ, Dodd PJ. CD4 count and tuberculosis risk in HIV-positive adults not on ART: a systematic review and meta-analysis. PeerJ 2017; 5.  https://doi.org/10.7717/peerj.4165PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Williams BG, Gouws E, Somse P et al (2015) Epidemiological trends for HIV in Southern Africa: implications for reaching the elimination targets. Curr HIV/AIDS Rep 12:196–206PubMedCrossRefGoogle Scholar
  38. 38.
    Williams BG, Korenromp EL, Gouws E, Schmid GP, Auvert B, Dye C (2006) HIV infection, antiretroviral therapy, and CD4+ cell count distributions in African populations. J Infect Dis 194:1450–1458PubMedCrossRefGoogle Scholar
  39. 39.
    Wolbers M, Babiker A, Sabin C et al (2010) Pretreatment CD4 Cell slope and progression to AIDS or death in HIV-infected patients initiating antiretroviral therapy—The CASCADE Collaboration: a collaboration of 23 cohort studies. PLoS Med 7:e1000239PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Touloumi G, Pantazis N, Pillay D et al (2013) Impact of HIV-1 subtype on CD4 count at HIV seroconversion, rate of decline, and viral load set point in European seroconverter cohorts. Clin Infect Dis 56:888–897PubMedCrossRefGoogle Scholar
  41. 41.
    Dodd PJ, Prendergast AJ, Beecroft C, Kampmann B, Seddon JA (2017) The impact of HIV and antiretroviral therapy on TB risk in children: a systematic review and meta-analysis. Thorax 72:559–575PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Dodd PJ, White RG, Corbett EL (2011) Periodic active case finding for TB: when to look? PLoS One 6:e29130PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Toossi Z, Mayanja-Kizza H, Hirsch CS et al (2001) Impact of tuberculosis (TB) on HIV-1 activity in dually infected patients. Clin Exp Immunol 123:233–238PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Samji H, Cescon A, Hogg RS et al (2013) Closing the gap: increases in life expectancy among treated HIV-positive individuals in the United States and Canada. PLoS One 8:e81355PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Tanser F, Bärnighausen T, Grapsa E, Zaidi J, Newell M-L (2013) High coverage of ART associated with decline in risk of HIV acquisition in rural KwaZulu-Natal, South Africa. Science 339:966–971PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Cohen MS, Chen YQ, McCauley M et al (2016) Antiretroviral therapy for the prevention of HIV-1 transmission. N Engl J Med 375:830–839PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Guideline on when to start antiretroviral therapy and on pre-exposure prophylaxis for HIV. Geneva: World Health Organization; 2015.Google Scholar
  48. 48.
    Suthar AB, Lawn SD, del Amo J et al (2012) Antiretroviral therapy for prevention of tuberculosis in adults with HIV: a systematic review and meta-analysis. PLoS Med 9:e1001270PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Lawn SD, Myer L, Edwards D, Bekker L-G, Wood R (2009) Short-term and long-term risk of tuberculosis associated with CD4 cell recovery during antiretroviral therapy in South Africa. AIDS 23:1717–1725PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Nicholas S, Sabapathy K, Ferreyra C, Varaine F, Pujades-Rodríguez M, AIDS Working Group of Médecins Sans Frontières (2011) Incidence of tuberculosis in HIV-infected patients before and after starting combined antiretroviral therapy in 8 sub-Saharan African HIV programs. J Acquir Immune Defic Syndr 57:311–318PubMedCrossRefGoogle Scholar
  51. 51.
    Gupta A, Wood R, Kaplan R, Bekker L-G, Lawn SD (2012) Tuberculosis incidence rates during 8 years of follow-up of an antiretroviral treatment cohort in South Africa: comparison with rates in the community. PLoS One 7:e34156PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    McIlleron H, Meintjes G, Burman WJ, Maartens G (2007) Complications of antiretroviral therapy in patients with tuberculosis: drug interactions, toxicity, and immune reconstitution inflammatory syndrome. J Infect Dis 196:S63–S75PubMedCrossRefGoogle Scholar
  53. 53.
    Nglazi MD, Bekker L-G, Wood R, Kaplan R (2015) The impact of HIV status and antiretroviral treatment on TB treatment outcomes of new tuberculosis patients attending co-located TB and ART services in South Africa: a retrospective cohort study. BMC Infect Dis 15:536PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Giri PA, Deshpande JD, Phalke DB (2013) Prevalence of pulmonary tuberculosis among HIV positive patients attending antiretroviral therapy clinic. N Am J Med Sci 5:367–370PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Recommendation on 36 months isoniazid preventive therapy to adults and adolescents living with HIV in resource-constrained and high TB- and HIV-prevalence settings: 2015 Update. World Health Organization, Geneva, p 2015Google Scholar
  56. 56.
    Akolo C, Adetifa I, Shepperd S, Volmink J (2010) Treatment of latent tuberculosis infection in HIV infected persons. Cochrane Database Syst Rev:CD000171
  57. 57.
    Golub JE, Saraceni V, Cavalcante SC et al (2007) The impact of antiretroviral therapy and isoniazid preventive therapy on tuberculosis incidence in HIV-infected patients in Rio de Janeiro, Brazil. AIDS 21:1441–1448PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Ayele HT, van Mourik MSM, Debray TPA, Bonten MJM (2015) Isoniazid prophylactic therapy for the prevention of tuberculosis in HIV infected adults: a systematic review and meta-analysis of randomized trials. PLoS One 10:e0142290PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Samandari T, Agizew TB, Nyirenda S et al (2011) 6-month versus 36-month isoniazid preventive treatment for tuberculosis in adults with HIV infection in Botswana: a randomised, double-blind, placebo-controlled trial. Lancet 377:1588–1598PubMedCrossRefGoogle Scholar
  60. 60.
    Houben RMGJ, Sumner T, Grant AD, White RG (2014) Ability of preventive therapy to cure latent Mycobacterium tuberculosis infection in HIV-infected individuals in high-burden settings. Proc Natl Acad Sci U S A 111:5325–5330PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Langley I, Lin H-H, Egwaga S et al (2014) Assessment of the patient, health system, and population effects of Xpert MTB/RIF and alternative diagnostics for tuberculosis in Tanzania: an integrated modelling approach. Lancet Glob Health 2:e581–e591PubMedCrossRefGoogle Scholar
  62. 62.
    Dowdy DW, Andrews JR, Dodd PJ, Gilman RH. A user-friendly, open-source tool to project impact and cost of diagnostic tests for tuberculosis. elife 2014; 3.  https://doi.org/10.7554/elife.02565
  63. 63.
    Basu S, Andrews JR, Poolman EM et al (2007) Prevention of nosocomial transmission of extensively drug-resistant tuberculosis in rural South African district hospitals: an epidemiological modelling study. Lancet 370:1500–1507PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Taylor JG, Yates TA, Mthethwa M, Tanser F, Abubakar I, Altamirano H (2016) Measuring ventilation and modelling M. tuberculosis transmission in indoor congregate settings, rural KwaZulu-Natal. Int J Tuberc Lung Dis 20:1155–1161PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Noakes CJ, Beggs CB, Sleigh PA (2004) Modelling the Performance of Upper Room Ultraviolet Germicidal Irradiation Devices in Ventilated Rooms: Comparison of Analytical and CFD Methods. Indoor Built Environ 13:477–488CrossRefGoogle Scholar
  66. 66.
    RMGJ H, Dowdy DW, Vassall A et al (2014) How can mathematical models advance tuberculosis control in high HIV prevalence settings? Int J Tuberc Lung Dis 18:509–514CrossRefGoogle Scholar
  67. 67.
    Bermejo A, Veeken H, Berra A (1992) Tuberculosis incidence in developing countries with high prevalence of HIV infection. AIDS 6:1203–1206PubMedCrossRefGoogle Scholar
  68. 68.
    Schulzer M (1992) An estimate of the future size of the tuberculosis problem in sub-Saharan Africa resulting from HIV infection. Tuber Lung Dis 73:52–58PubMedCrossRefGoogle Scholar
  69. 69.
    Dolin PJ, Raviglione MC, Kochi A (1994) Global tuberculosis incidence and mortality during 1990-2000. Bull World Health Organ 72:213–220PubMedPubMedCentralGoogle Scholar
  70. 70.
    Schulzer M, Radhamani MP, Grzybowski S, Mak E, Fitzgerald JM (1994) A mathematical model for the prediction of the impact of HIV infection on tuberculosis. Int J Epidemiol 23:400–407PubMedCrossRefGoogle Scholar
  71. 71.
    Massad E, Burattini MN, Coutinho FAB, Yang HM, Raimundo SM (1993) Modeling the interaction between aids and tuberculosis. Math Comput Model 17:7–21CrossRefGoogle Scholar
  72. 72.
    Naresh R, Sharma D, Tripathi A (2009) Modelling the effect of tuberculosis on the spread of HIV infection in a population with density-dependent birth and death rate. Math Comput Model 50:1154–1166CrossRefGoogle Scholar
  73. 73.
    Roeger L-IW, Feng Z, Castillo-Chavez C (2009) Modeling TB and HIV co-infections. Math Biosci Eng 6:815–837CrossRefPubMedGoogle Scholar
  74. 74.
    Kapitanov G (2015) A double age-structured model of the co-infection of tuberculosis and HIV. Math Biosci Eng 12:23–40PubMedCrossRefGoogle Scholar
  75. 75.
    Basu S, Orenstein E, Galvani AP (2008) The theoretical influence of immunity between strain groups on the progression of drug-resistant tuberculosis epidemics. J Infect Dis 198:1502–1513PubMedCrossRefGoogle Scholar
  76. 76.
    Basu S, Galvani AP (2009) The evolution of tuberculosis virulence. Bull Math Biol 71:1073–1088PubMedCrossRefGoogle Scholar
  77. 77.
    Sergeev R, Colijn C, Murray M, Cohen T (2012) Modeling the dynamic relationship between HIV and the risk of drug-resistant tuberculosis. Sci Transl Med 4:135ra67PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Porco TC, Small PM, Blower SM (2001) Amplification dynamics: predicting the effect of HIV on tuberculosis outbreaks. J Acquir Immune Defic Syndr 28:437–444PubMedCrossRefGoogle Scholar
  79. 79.
    Murray M (2002) Determinants of cluster distribution in the molecular epidemiology of tuberculosis. Proc Natl Acad Sci U S A 99:1538–1543PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Pretorius C, Dodd P, Wood R (2011) An investigation into the statistical properties of TB episodes in a South African community with high HIV prevalence. J Theor Biol 270:154–163PubMedCrossRefGoogle Scholar
  81. 81.
    Escombe AR, DAJ M, Gilman RH et al (2008) The infectiousness of tuberculosis patients coinfected with HIV. PLoS Med 5:e188PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Wood R, Johnstone-Robertson S, Uys P et al (2010) Tuberculosis transmission to young children in a South African community: modeling household and community infection risks. Clin Infect Dis 51:401–408PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Uys P, Marais BJ, Johnstone-Robertson S, Hargrove J, Wood R (2011) Transmission elasticity in communities hyperendemic for tuberculosis. Clin Infect Dis 52:1399–1404PubMedCrossRefGoogle Scholar
  84. 84.
    Andrews JR, Morrow C, Walensky RP, Wood R (2014) Integrating social contact and environmental data in evaluating tuberculosis transmission in a South African township. J Infect Dis 210:597–603PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Andrews JR, Morrow C, Wood R (2013) Modeling the role of public transportation in sustaining tuberculosis transmission in South Africa. Am J Epidemiol 177:556–561PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Dodd PJ, Looker C, Plumb ID et al (2016) Age- and sex-specific social contact patterns and incidence of Mycobacterium tuberculosis infection. Am J Epidemiol 183:156–166PubMedGoogle Scholar
  87. 87.
    Hughes G, Currie C, Corbett E. Modeling tuberculosis in areas of High HIV prevalence. In: Proceedings of the 2006 Winter Simulation Conference. 2006.  https://doi.org/10.1109/wsc.2006.323116CrossRefGoogle Scholar
  88. 88.
    Sánchez MS, Lloyd-Smith JO, Williams BG et al (2009) Incongruent HIV and tuberculosis co-dynamics in Kenya: interacting epidemics monitor each other. Epidemics 1:14–20PubMedCrossRefGoogle Scholar
  89. 89.
    Blaser N, Zahnd C, Hermans S et al (2016) Tuberculosis in Cape Town: An age-structured transmission model. Epidemics 14:54–61PubMedCrossRefGoogle Scholar
  90. 90.
    Pretorius C, Glaziou P, Dodd PJ, White R, Houben R (2014) Using the TIME model in Spectrum to estimate tuberculosis-HIV incidence and mortality. AIDS (28 Suppl 4):S477–S487PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Agusto FB, Adekunle AI (2014) Optimal control of a two-strain tuberculosis-HIV/AIDS co-infection model. Biosystems 119:20–44PubMedCrossRefGoogle Scholar
  92. 92.
    Kaur N, Ghosh M, Bhatia SS (2014) The role of screening and treatment in the transmission dynamics of HIV/AIDS and tuberculosis co-infection: a mathematical study. J Biol Phys 40:139–166PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Sharomi O, Podder CN, Gumel AB, Song B (2008) Mathematical analysis of the transmission dynamics of HIV/TB coinfection in the presence of treatment. Math Biosci Eng 5:145–174CrossRefPubMedGoogle Scholar
  94. 94.
    Bacaër N, Ouifki R, Pretorius C, Wood R, Williams B (2008) Modeling the joint epidemics of TB and HIV in a South African township. J Math Biol 57:557–593PubMedCrossRefGoogle Scholar
  95. 95.
    Wallengren K, Scano F, Nunn P, Margot B, Buthelezi S, Williams B, Pym A, Samuel EY, Mirzayev F, Nkhoma W, Mvusi L, Pillay Y. Resistance to TB drugs in KwaZulu-Natal: causes and prospects for control. 2011. https://arxiv.org/pdf/1107.1800.pdf.
  96. 96.
    Basu S, Friedland GH, Medlock J et al (2009) Averting epidemics of extensively drug-resistant tuberculosis. Proc Natl Acad Sci U S A 106:7672–7677PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Basu S, Stuckler D, McKee M (2011) Addressing institutional amplifiers in the dynamics and control of tuberculosis epidemics. Am J Trop Med Hyg 84:30–37PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Heymann SJ (1993) Modelling the efficacy of prophylactic and curative therapies for preventing the spread of tuberculosis in Africa. Trans R Soc Trop Med Hyg 87:406–411PubMedCrossRefGoogle Scholar
  99. 99.
    Guwatudde D, Debanne SM, Diaz M, King C, Whalen CC (2004) A re-examination of the potential impact of preventive therapy on the public health problem of tuberculosis in contemporary sub-Saharan Africa. Prev Med 39:1036–1046PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Cohen T, Lipsitch M, Walensky RP, Murray M (2006) Beneficial and perverse effects of isoniazid preventive therapy for latent tuberculosis infection in HIV-tuberculosis coinfected populations. Proc Natl Acad Sci U S A 103:7042–7047PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Basu S, Maru D, Poolman E, Galvani A (2009) Primary and secondary tuberculosis preventive treatment in HIV clinics: simulating alternative strategies. Int J Tuberc Lung Dis 13:652–658PubMedGoogle Scholar
  102. 102.
    Mills HL, Cohen T, Colijn C (2011) Modelling the performance of isoniazid preventive therapy for reducing tuberculosis in HIV endemic settings: the effects of network structure. J R Soc Interface 8:1510–1520PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Kunkel A, Crawford FW, Shepherd J, Cohen T (2016) Benefits of continuous isoniazid preventive therapy may outweigh resistance risks in a declining tuberculosis/HIV coepidemic. AIDS 30:2715–2723PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Baltussen R, Floyd K, Dye C (2005) Cost effectiveness analysis of strategies for tuberculosis control in developing countries. BMJ 331:1364PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Laxminarayan R, Klein EY, Darley S, Adeyi O (2009) Global investments in TB control: economic benefits. Health Aff 28:w730–w742CrossRefGoogle Scholar
  106. 106.
    Sánchez MS, Lloyd-Smith JO, Porco TC et al (2008) Impact of HIV on novel therapies for tuberculosis control. AIDS 22:963–972PubMedCrossRefGoogle Scholar
  107. 107.
    Dowdy DW, Chaisson RE (2009) The persistence of tuberculosis in the age of DOTS: reassessing the effect of case detection. Bull World Health Organ 87:296–304PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Mellor GR, Currie CSM, Corbett EL (2011) Incorporating household structure into a discrete-event simulation model of tuberculosis and HIV. ACM Trans Model Comput Simul 21:1–17CrossRefGoogle Scholar
  109. 109.
    Yaesoubi R, Cohen T (2013) Identifying dynamic tuberculosis case-finding policies for HIV/TB coepidemics. Proc Natl Acad Sci U S A 110:9457–9462PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Azman AS, Golub JE, Dowdy DW. How much is tuberculosis screening worth? Estimating the value of active case finding for tuberculosis in South Africa, China, and India. BMC Med 2014; 12  https://doi.org/10.1186/s12916-014-0216-0
  111. 111.
    Dowdy DW, Chaisson RE, Moulton LH, Dorman SE (2006) The potential impact of enhanced diagnostic techniques for tuberculosis driven by HIV: a mathematical model. AIDS 20:751–762PubMedCrossRefGoogle Scholar
  112. 112.
    Menzies NA, Cohen T, Lin H-H, Murray M, Salomon JA (2012) Population health impact and cost-effectiveness of tuberculosis diagnosis with Xpert MTB/RIF: a dynamic simulation and economic evaluation. PLoS Med 9:e1001347PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Lin H-H, Langley I, Mwenda R et al (2011) A modelling framework to support the selection and implementation of new tuberculosis diagnostic tools. Int J Tuberc Lung Dis 15:996–1004PubMedCrossRefGoogle Scholar
  114. 114.
    Langley I, Doulla B, Lin H-H, Millington K, Squire B (2012) Modelling the impacts of new diagnostic tools for tuberculosis in developing countries to enhance policy decisions. Health Care Manag Sci 15:239–253PubMedCrossRefGoogle Scholar
  115. 115.
    Williams BG, Granich R, Chauhan LS, Dharmshaktu NS, Dye C (2005) The impact of HIV/AIDS on the control of tuberculosis in India. Proc Natl Acad Sci U S A 102:9619–9624PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Granich RM, Gilks CF, Dye C, De Cock KM, Williams BG (2009) Universal voluntary HIV testing with immediate antiretroviral therapy as a strategy for elimination of HIV transmission: a mathematical model. Lancet 373:48–57CrossRefPubMedGoogle Scholar
  117. 117.
    Bhunu CP, Garira W, Mukandavire Z (2009) Modeling HIV/AIDS and tuberculosis coinfection. Bull Math Biol 71:1745–1780PubMedCrossRefGoogle Scholar
  118. 118.
    Dodd PJ, Knight GM, Lawn SD, Corbett EL, White RG (2013) Predicting the long-term impact of antiretroviral therapy scale-up on population incidence of tuberculosis. PLoS One 8:e75466PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Pretorius C, Menzies NA, Chindelevitch L et al (2014) The potential effects of changing HIV treatment policy on tuberculosis outcomes in South Africa: results from three tuberculosis-HIV transmission models. AIDS (28 Suppl 1):S25–S34PubMedCrossRefGoogle Scholar
  120. 120.
    Currie CSM, Williams BG, Cheng RCH, Dye C (2003) Tuberculosis epidemics driven by HIV: is prevention better than cure? AIDS 17:2501–2508PubMedCrossRefGoogle Scholar
  121. 121.
    Currie CSM, Floyd K, Williams BG, Dye C (2005) Cost, affordability and cost-effectiveness of strategies to control tuberculosis in countries with high HIV prevalence. BMC Public Health 5:130PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Chindelevitch L, Menzies NA, Pretorius C, Stover J, Salomon JA, Cohen T. Evaluating the potential impact of enhancing HIV treatment and tuberculosis control programmes on the burden of tuberculosis. J R Soc Interface 2015; 12  https://doi.org/10.1098/rsif.2015.0146PubMedCentralCrossRefGoogle Scholar
  123. 123.
    Knight GM, Dodd PJ, Grant AD, Fielding KL, Churchyard GJ, White RG (2015) Tuberculosis prevention in South Africa. PLoS One 10:e0122514PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Gilbert JA, Long EF, Brooks RP et al (2015) Integrating community-based interventions to reverse the convergent TB/HIV epidemics in rural South Africa. PLoS One 10:e0126267PubMedPubMedCentralCrossRefGoogle Scholar
  125. 125.
    Gilbert JA, Shenoi SV, Moll AP, Friedland GH, Paltiel AD, Galvani AP (2016) Cost-Effectiveness of Community-Based TB/HIV Screening and Linkage to Care in Rural South Africa. PLoS One 11:e0165614PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Eaton JW, Menzies NA, Stover J et al (2014) Health benefits, costs, and cost-effectiveness of earlier eligibility for adult antiretroviral therapy and expanded treatment coverage: a combined analysis of 12 mathematical models. Lancet Glob Health 2:e23–e34PubMedCrossRefGoogle Scholar
  127. 127.
    RMGJ H, Menzies NA, Sumner T et al (2016) Feasibility of achieving the 2025 WHO global tuberculosis targets in South Africa, China, and India: a combined analysis of 11 mathematical models. Lancet Glob Health 4:e806–e815CrossRefGoogle Scholar
  128. 128.
    Trauer JM, Ragonnet R, Doan TN, McBryde ES (2017) Modular programming for tuberculosis control, the ‘AuTuMN’ platform. BMC Infect Dis 17:546PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    RMGJ H, Lalli M, Sumner T et al (2016) TIME Impact - a new user-friendly tuberculosis (TB) model to inform TB policy decisions. BMC Med 14:56CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.School of Health and Related Research, University of SheffieldSheffieldUK
  2. 2.Avenir HealthGlastonburyUSA
  3. 3.South African Centre for Epidemiological Modelling and Analysis, University of StellenboschStellenboschSouth Africa

Personalised recommendations