Viral kinetic modeling: state of the art

Journal of Pharmacokinetics and Pharmacodynamics - Tập 41 - Trang 431-443 - 2014
Laetitia Canini1, Alan S. Perelson1
1Theoretical Biology and Biophysics, MS-K710, Los Alamos National Laboratory, Los Alamos, USA

Tóm tắt

Viral kinetic (VK) modeling has led to increased understanding of the within host dynamics of viral infections and the effects of therapy. Here we review recent developments in the modeling of viral infection kinetics with emphasis on two infectious diseases: hepatitis C and influenza. We review how VK modeling has evolved from simple models of viral infections treated with a drug or drug cocktail with an assumed constant effectiveness to models that incorporate drug pharmacokinetics and pharmacodynamics, as well as phenomenological models that simply assume drugs have time varying-effectiveness. We also discuss multiscale models that include intracellular events in viral replication, models of drug-resistance, models that include innate and adaptive immune responses and models that incorporate cell-to-cell spread of infection. Overall, VK modeling has provided new insights into the understanding of the disease progression and the modes of action of several drugs. We expect that VK modeling will be increasingly used in the coming years to optimize drug regimens in order to improve therapeutic outcomes and treatment tolerability for infectious diseases.

Tài liệu tham khảo

Ho DD et al (1995) Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373(6510):123–126 Perelson AS (2002) Modelling viral and immune system dynamics. Nat Rev Immunol 2(1):28–36 Perelson AS et al (1997) Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387:188–191 Perelson AS et al (1996) HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271(5255):1582–1586 Wei X et al (1995) Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373(6510):117–122 Neumann AU et al (1998) Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science 282(5386):103–107 Ciupe SM et al (2007) The role of cells refractory to productive infection in acute hepatitis B viral dynamics. Proc Natl Acad Sci USA 104(12):5050–5055 Ciupe SM et al (2007) Modeling the mechanisms of acute hepatitis B virus infection. J Theor Biol 247(1):23–35 Dahari H et al (2009) Modeling complex decay profiles of hepatitis B virus during antiviral therapy. Hepatology 49(1):32–38 Lewin SR et al (2001) Analysis of hepatitis B viral load decline under potent therapy: complex decay profiles observed. Hepatology 34(5):1012–1020 Murray JM et al (2005) Dynamics of hepatitis B virus clearance in chimpanzees. Proc Natl Acad Sci USA 102(49):17780–17785 Nowak MA et al (1996) Viral dynamics in hepatitis B virus infection. Proc Natl Acad Sci USA 93(9):4398–4402 Ribeiro RM et al (2010) Hepatitis B virus kinetics under antiviral therapy sheds light on differences in hepatitis B e antigen positive and negative infections. J Infect Dis 202(9):1309–1318 Ribeiro RM, Lo A, Perelson AS (2002) Dynamics of hepatitis B virus infection. Microb Infect 4(8):829–835 Emery VC, Griffiths PD (2000) Prediction of cytomegalovirus load and resistance patterns after antiviral chemotherapy. Proc Natl Acad Sci USA 97(14):8039–8044 Emery VC et al (2012) Differential decay kinetics of human cytomegalovirus glycoprotein B genotypes following antiviral chemotherapy. J Clin Virol 54(1):56–60 Regoes RR et al (2006) Modelling cytomegalovirus replication patterns in the human host: factors important for pathogenesis. Proc R Soc B 273(1596):1961–1967 Schiffer JT, Corey L (2013) Rapid host immune response and viral dynamics in herpes simplex virus-2 infection. Nat Med 19(3):280–288 Schiffer JT et al (2013) Rapid localized spread and immunologic containment define Herpes simplex virus-2 reactivation in the human genital tract. Elife 2:e00288 Schiffer JT et al (2011) The kinetics of mucosal herpes simplex virus-2 infection in humans: evidence for rapid viral–host interactions. J Infect Dis 204(4):554–561 Baccam P et al (2006) Kinetics of influenza A virus infection in humans. J Virol 80(15):7590–7599 Beauchemin C, Samuel J, Tuszynski J (2005) A simple cellular automaton model for influenza A viral infections. J Theor Biol 232(2):223–234 Bocharov GA, Romanyukha AA (1994) Mathematical model of antiviral immune response. III. Influenza A virus infection. J Theor Biol 167(4):323–360 Canini L, Carrat F (2011) Population modeling of influenza A/H1N1 virus kinetics and symptom dynamics. J Virol 85(6):2764–2770 Hancioglu B, Swigon D, Clermont G (2007) A dynamical model of human immune response to influenza A virus infection. J Theor Biol 246(1):70–86 Handel A, Longini IM Jr, Antia R (2010) Towards a quantitative understanding of the within-host dynamics of influenza A infections. J R Soc Interface 7(42):35–47 Miao H et al (2010) Quantifying the early immune response and adaptive immune response kinetics in mice infected with influenza A virus. J Virol 84(13):6687–6698 Pawelek KA et al (2012) Modeling within-host dynamics of influenza virus infection including immune responses. PLoS Comput Biol 8(6):e1002588 Saenz RA et al (2010) Dynamics of influenza virus infection and pathology. J Virol 84(8):3974–3983 Smith AM et al (2011) Effect of 1918 PB1-F2 expression on influenza A virus infection kinetics. PLoS Comput Biol 7(2):e1001081 Smith AM, Perelson AS (2011) Influenza A virus infection kinetics: quantitative data and models. Wiley Interdiscip Rev Syst Biol Med 3(4):429–445 Perelson AS, Rong L, Hayden FG (2012) Combination antiviral therapy for influenza: predictions from modeling of human infections. J Infect Dis 205(11):1642–1645 Murillo LN, Murillo MS, Perelson AS (2013) Towards multiscale modeling of influenza infection. J Theor Biol 332:267–290 Smith AM et al (2013) Kinetics of coinfection with influenza A virus and Streptococcus pneumoniae. PLoS Pathog 9(3):e1003238 Asquith B, Bangham CR (2007) Quantifying HTLV-I dynamics. Immunol Cell Biol 85(4):280–286 Heffernan J, Keeling MJ (2008) An in-host model of acute infection: measles as a case study. Theor Popul Biol 73(1):134–147 Zhang J et al (2013) Modeling the acute and chronic phases of Theiler murine encephalomyelitis virus infection. J Virol 87(7):4052–4059 Snoeck E et al (2010) A comprehensive hepatitis C viral kinetic model explaining cure. Clin Pharmacol Ther 87(6):706–713 Guedj J et al (2014) Modeling viral kinetics and treatment outcome during alisporivir interferon-free treatment in HCV genotype 2/3 patients. Hepatology 59(5):1706–1714 Gao M et al (2010) Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect. Nature 465(7294):96–100 Beauchemin CA et al (2008) Modeling amantadine treatment of influenza A virus in vitro. J Theor Biol 254(2):439–451 Bochud P-Y et al (2011) IL28B polymorphisms predict reduction of HCV RNA from the first day of therapy in chronic hepatitis C. J Hepatol 55(5):980–988 Dahari H et al (2011) Hepatitis C viral kinetics in the era of direct acting antiviral agents and interleukin-28B. Curr Hepat Rep 10(3):214–227 Guedj H et al (2012) The impact of fibrosis and steatosis on early viral kinetics in HCV genotype 1-infected patients treated with PEG-IFN-alfa-2a and ribavirin. J Viral Hepat 19(7):488–496 Guedj J et al (2012) Understanding silibinin’s modes of action against HCV using viral kinetic modeling. J Hepatol 56(5):1019–1024 Lagging M et al (2011) Response prediction in chronic hepatitis C by assessment of IP-10 and IL28B-related single nucleotide polymorphisms. PLoS ONE 6(2):e17232 Layden-Almer JE et al (2003) Viral dynamics and response differences in HCV-infected African American and white patients treated with IFN and ribavirin. Hepatology 37(6):1343–1350 Neumann AU et al (2000) Differences in viral dynamics between genotypes 1 and 2 of hepatitis C virus. J Infect Dis 182(1):28–35 Herrmann E et al (2003) Effect of ribavirin on hepatitis C viral kinetics in patients treated with pegylated interferon. Hepatology 37(6):1351–1358 Dahari H, Ribeiro RM, Perelson AS (2007) Triphasic decline of hepatitis C virus RNA during antiviral therapy. Hepatology 46(1):16–21 Dahari H et al (2007) Modeling hepatitis C virus dynamics: liver regeneration and critical drug efficacy. J Theor Biol 247(2):371–381 Rong L et al (2010) Rapid emergence of protease inhibitor resistance in hepatitis C virus. Sci Transl Med 2(30):30ra32 Dahari H et al (2010) Pharmacodynamics of PEG-IFN-alpha-2a in HIV/HCV co-infected patients: implications for treatment outcomes. J Hepatol 53(3):460–467 Guedj J et al (2010) A perspective on modelling hepatitis C virus infection. J Viral Hepat 17(12):825–833 Shudo E, Ribeiro RM, Perelson AS (2009) Modeling HCV kinetics under therapy using PK and PD information. Expert Opin Drug Metab Toxicol 5(3):321–332 Talal AH et al (2006) Pharmacodynamics of PEG-IFN α differentiate HIV/HCV coinfected sustained virological responders from nonresponders. Hepatology 43(5):943–953 Adiwijaya BS et al (2012) A viral dynamic model for treatment regimens with direct-acting antivirals for chronic hepatitis C infection. PLoS Comput Biol 8(1):e1002339 Powers KA et al (2003) Modeling viral and drug kinetics: hepatitis C virus treatment with pegylated interferon alfa-2b. Semin Liver Dis 23:13–18 Holford NH, Sheiner LB (1981) Understanding the dose–effect relationship. Clin Pharmacokinet 6(6):429–453 Guedj J et al (2012) Hepatitis C viral kinetics with the nucleoside polymerase inhibitor mericitabine (RG7128). Hepatology 55(4):1030–1037 Shudo E et al (2008) A hepatitis C viral kinetic model that allows for time-varying drug effectiveness. Antivir Ther 13(7):919–926 Shudo E, Ribeiro R, Perelson A (2008) Modelling the kinetics of hepatitis C virus RNA decline over 4 weeks of treatment with pegylated interferon α-2b. J Viral Hepat 15(5):379–382 Conway JM, Perelson AS (2014). Hepatitis C virus infection model with time-varying drug effectivenss: solution and analysis (submitted) Guedj J et al (2014) Analysis of the hepatitis C viral kinetics during administration of two nucleotide analogues: sofosbuvir (GS-7977) and GS-0938. Antivir Ther 19(2):211–220 Greco WR, Bravo G, Parsons JC (1995) The search for synergy: a critical review from a response surface perspective. Pharmacol Rev 47(2):331–385 Ribeiro RM et al (2012) Quantifying the diversification of hepatitis C virus (HCV) during primary infection: estimates of the in vivo mutation rate. PLoS Pathog 8(8):e1002881 Drake JW et al (1998) Rates of spontaneous mutation. Genetics 148(4):1667–1686 Kieffer T et al (2007) Evaluation of viral variants during a Phase 2 study (PROVE2) of telaprevir with peginterferon alfa-2a and ribavirin in treatment-naive HCV genotype 1-infected patients. Hepatology 46(Suppl 1):862 Rong L, Ribeiro RM, Perelson AS (2012) Modeling quasispecies and drug resistance in hepatitis C patients treated with a protease inhibitor. Bull Math Biol 74(8):1789–1817 Adiwijaya BS et al (2010) A multi-variant, viral dynamic model of genotype 1 HCV to assess the in vivo evolution of protease-inhibitor resistant variants. PLoS Comput Biol 6(4):e1000745 Guedj J et al (2013) Modeling shows that the NS5A inhibitor daclatasvir has two modes of action and yields a shorter estimate of the hepatitis C virus half-life. Proc Natl Acad Sci USA 110(10):3991–3996 Rong L, Perelson AS (2013) Mathematical analysis of multiscale models for hepatitis C virus dynamics under therapy with direct-acting antiviral agents. Math Biosci 245(1):22–30 Rong L et al (2013) Analysis of hepatitis C virus decline during treatment with the protease inhibitor danoprevir using a multiscale model. PLoS Comput Biol 9(3):e1002959 Kandathil AJ et al (2013) Use of laser capture microdissection to map hepatitis C virus-positive hepatocytes in human liver. Gastroenterology 145(6):1404.e10–1413.e10 Graw F et al (2014) Inferring viral dynamics in chronically HCV infected patients from the spatial distribution of infected hepatocytes (submitted) Graw F, Perelson AS (2013) Spatial aspects of HIV infection. In: Mathematical methods and models in biomedicine. Springer, Berlin, pp 3–31 Bauer AL, Beauchemin CA, Perelson AS (2009) Agent-based modeling of host–pathogen systems: the successes and challenges. Inf Sci 179(10):1379–1389 Chao DL et al (2010) FluTE, a publicly available stochastic influenza epidemic simulation model. PLoS Comput Biol 6(1):e1000656 Ferguson NM et al (2005) Strategies for containing an emerging influenza pandemic in Southeast Asia. Nature 437(7056):209–214 Mills CE, Robins JM, Lipsitch M (2004) Transmissibility of 1918 pandemic influenza. Nature 432(7019):904–906 Jansen CA et al (2013) Differential lung NK cell responses in avian influenza virus infected chickens correlate with pathogenicity. Sci Rep 3:2478 Pommerenke C et al (2012) Global transcriptome analysis in influenza-infected mouse lungs reveals the kinetics of innate and adaptive host immune responses. PLoS ONE 7(7):e41169 Belz GT et al (2002) Compromised influenza virus-specific CD8+-T-cell memory in CD4+-T-cell-deficient mice. J Virol 76(23):12388–12393 Tridane A, Kuang Y (2010) Modeling the interaction of cytotoxic T lymphocytes and influenza virus infected epithelial cells. Math Biosci Eng 7(1):171–185 Ginaldi L et al (2001) Immunosenescence and infectious diseases. Microbes Infect 3(10):851–857 Hernandez-Vargas EA et al (2014) The effects of aging on influenza virus infection dynamics. J Virol 88(8):4123–4131 Hayden FG et al (1998) Local and systemic cytokine responses during experimental human influenza A virus infection. Relation to symptom formation and host defense. J Clin Investig 101(3):643 Anderson RM, May RM (1982) Directly transmitted infectious diseases: control by vaccination. Science 215(4536):1053–1060 Handel A, Longini IM Jr, Antia R (2007) Neuraminidase inhibitor resistance in influenza: assessing the danger of its generation and spread. PLoS Comput Biol 3(12):e240 Canini L et al (2014) Impact of different oseltamivir regimens on treating influenza A virus infection and resistance emergence: insights from a modelling study. PLoS Comput Biol 10(4):e1003568 Heldt FS et al (2013) Multiscale modeling of influenza A virus infection supports the development of direct-acting antivirals. PLoS Comput Biol 9(11):e1003372 Guedj J, Perelson AS (2011) Second-phase hepatitis C virus RNA decline during telaprevir-based therapy increases with drug effectiveness: implications for treatment duration. Hepatology 53(6):1801–1808 Adiwijaya BS et al (2011) Modeling clinical and virology data from phase 2 and 3 studies support 12-week telaprevir duration in combination with 24- or 48-week peginterferon/ribavirin. Gastroenterology 140(5):943 Kohli A et al (2014) Hepatitis C antiviral therapy for 6 or 12 weeks: final results of the SYNERGY trial. In: Conference on retroviruses and opportunistic infections, 2014 Wieland S et al (2014) Simultaneous detection of hepatitis C virus and interferon stimulated gene expression in infected human liver. Hepatology 59(6):2121–2130 Sidharthan S et al (2014) Predicting response to all-oral directly acting antiviral therapy for hepatitis C using results of Roche and Abbott HCV viral load assays. Hepatol Int 8(S1):S227–S228 Cowling BJ et al (2010) Comparative epidemiology of pandemic and seasonal influenza A in households. N Engl J Med 362(23):2175–2184 Atkinson A, Donev A (1992) Optimum experimental designs. Clarendon, Oxford Canini L, Carrat F (2011) Viral kinetics studies on influenza: when and how many times are nasal samples to be collected? Influenza Other Respir Viruses 5(S1):144–147 Gustin KM et al (2011) Influenza virus aerosol exposure and analytical system for ferrets. Proc Natl Acad Sci USA 108(20):8432–8437 Eccles R (2005) Understanding the symptoms of the common cold and influenza. Lancet Infect Dis 5(11):718–725