A Multi-scale Analysis of Influenza A Virus Fitness Trade-offs due to Temperature-dependent Virus Persistence

PLoS Computational Biology

Volumn 9, Issue 3, 2013, Pages

  Handel, Andreas ^a   Brown, Justin ^a   Stallknecht, David ^a   Rohani, Pejman ^b,c  

^a UNIVERSITY OF GEORGIA   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECONOMIC AND SOCIAL EFFECTS; HEALTH; IMMUNE SYSTEM;

AVIAN INFLUENZA; DIFFERENTIAL PRESSURES; IMMUNE RESPONSE; INFLUENZA A VIRUS; INFLUENZA VIRUS; LOWS-TEMPERATURES; MULTI SCALE ANALYSIS; SELECTION PRESSURES; TEMPERATURE DEPENDENT; TRADE OFF;

VIRUSES;

ARTICLE; CONTROLLED STUDY; HIGH TEMPERATURE; IMMUNE RESPONSE; INFECTION RATE; INFLUENZA VIRUS A; LOW TEMPERATURE; MATHEMATICAL MODEL; NONHUMAN; PERSISTENT VIRUS INFECTION; TEMPERATURE DEPENDENCE; TEMPERATURE SENSITIVITY; VIRAL CLEARANCE; VIRUS CELL INTERACTION; VIRUS LOAD; VIRUS SHEDDING; VIRUS STRAIN; VIRUS TRANSMISSION; VIRUS VIRULENCE;

EID: 84875977734     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002989     Document Type: Article

References (89)

1. Cox NJ, Subbarao K, (2000) Global epidemiology of influenza: past and present. Annu Rev Med 51: 407-421.
2. Nicholson KG, Wood JM, Zambon M, (2003) Influenza. The Lancet 362: 1733-1745.
3. Taubenberger JK, Morens DM, (2008) The pathology of influenza virus infections. Annu Rev Pathol 3: 499-522.
4. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, et al. (2003) Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289: 179-186.
5. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y, (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56: 152-179.
6. Horimoto T, Kawaoka Y, (2005) Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 3: 591-600.
7. Lewis DB, (2006) Avian flu to human influenza. Annu Rev Med 57: 139-154.
8. Palese P, (2004) Influenza: old and new threats. Nature Medicine 10: S82-S87.
9. Mideo N, Alizon S, Day T, (2008) Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol Evol 23: 511-517.
10. Alizon S, Luciani F, Regoes RR, (2011) Epidemiological and clinical consequences of within-host evolution. Trends Microbiol 19: 24-32.
11. Reperant LA, Kuiken T, Grenfell BT, Osterhaus ADME, Dobson AP, (2012) Linking influenza virus tissue tropism to population-level reproductive fitness. PLoS One 7: e43115.
12. Belshe RB, Mendelman PM, Treanor J, King J, Gruber WC, et al. (1998) The efficacy of live attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine in children. N Engl J Med 338: 1405-1412.
13. Cox RJ, Brokstad KA, Ogra P, (2004) Influenza virus: immunity and vaccination strategies. comparison of the immune response to inactivated and live, attenuated influenza vaccines. Scand J Immunol 59: 1-15.
14. Lowen AC, Mubareka S, Steel J, Palese P, (2007) Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog 3: 1470-1476.
15. Scull MA, Gillim-Ross L, Santos C, Roberts KL, Bordonali E, et al. (2009) Avian influenza virus glycoproteins restrict virus replication and spread through human airway epithelium at temperatures of the proximal airways. PLoS Pathog 5: e1000424.
16. Breban R, Drake JM, Stallknecht DE, Rohani P, (2009) The role of environmental transmission in recurrent avian influenza epidemics. PLoS Comput Biol 5: e1000346.
17. Rohani P, Breban R, Stallknecht DE, Drake JM, (2009) Environmental transmission of low pathogenicity avian influenza viruses and its implications for pathogen invasion. Proc Natl Acad Sci U S A 106: 10365-10369.
18. Breban R, Drake JM, Rohani P, (2010) A general multi-strain model with environmental transmission: invasion conditions for the disease-free and endemic states. J Theor Biol 264: 729-736.
19. Roche B, Lebarbenchon C, Gauthier-Clerc M, Chang CM, Thomas F, et al. (2009) Water-borne transmission drives avian influenza dynamics in wild birds: the case of the 2005-2006 epidemics in the camargue area. Infect Genet Evol 9: 800-805.
20. Farnsworth ML, Miller RS, Pedersen K, Lutman MW, Swafford SR, et al. (2012) Environmental and demographic determinants of avian influenza viruses in waterfowl across the contiguous united states. PLoS One 7: e32729.
21. Lebarbenchon C, Yang M, Keeler SP, Ramakrishnan MA, Brown JD, et al. (2011) Viral replication, persistence in water and genetic characterization of two influenza a viruses isolated from surface lake water. PLoS One 6: e26566.
22. Hnaux V, Samuel MD, Bunck CM, (2010) Model-based evaluation of highly and low pathogenic avian influenza dynamics in wild birds. PLoS One 5: e10997.
23. Hnaux V, Samuel MD, (2011) Avian influenza shedding patterns in waterfowl: implications for surveillance, environmental transmission, and disease spread. J Wildl Dis 47: 566-578.
24. Stallknecht DE, Goekjian VH, Wilcox BR, Poulson RL, Brown JD, (2010) Avian influenza virus in aquatic habitats: what do we need to learn? Avian Dis 54: 461-465.
25. Atkinson MP, Wein LM, (2008) Quantifying the routes of transmission for pandemic influenza. Bull Math Biol 70: 820-867.
26. Nicas M, Jones RM, (2009) Relative contributions of four exposure pathways to influenza infection risk. Risk Anal 29: 1292-1303.
27. Wagner BG, Coburn BJ, Blower S, (2009) Calculating the potential for within-ight transmission of influenza a (h1n1). BMC Med 7: 81.
28. Weber TP, Stilianakis NI, (2008) Inactivation of influenza a viruses in the environment and modes of transmission: a critical review. J Infect 57: 361-373.
29. Tang JW, (2009) The effect of environmental parameters on the survival of airborne infectious agents. J R Soc Interface 6 (Suppl 6):: S737-S746.
30. Stallknecht DE, Kearney MT, Shane SM, Zwank PJ, (1990) Effects of ph, temperature, and salinity on persistence of avian influenza viruses in water. Avian Dis 34: 412-418.
31. Stallknecht DE, Shane SM, Kearney MT, Zwank PJ, (1990) Persistence of avian influenza viruses in water. Avian Dis 34: 406-411.
32. Brown JD, Swayne DE, Cooper RJ, Burns RE, Stallknecht DE, (2007) Persistence of h5 and h7 avian influenza viruses in water. Avian Dis 51: 285-289.
33. Brown JD, Goekjian G, Poulson R, Valeika S, Stallknecht DE, (2009) Avian influenza virus in water: infectivity is dependent on ph, salinity and temperature. Vet Microbiol 136: 20-26.
34. Bonhoeffer S, Lenski RE, Ebert D, (1996) The curse of the pharaoh: the evolution of virulence in pathogens with long living propagules. Proc Biol Sci 263: 715-721.
35. Gandon S, (1998) The curse of the pharaoh hypothesis. Proc Biol Sci 265: 1545-1552.
36. Day T, (2002) Virulence evolution via host exploitation and toxin production in spore-producing pathogens. Ecology Letters 5: 471-476.
37. Handel A, Bennett MR, (2008) Surviving the bottleneck: transmission mutants and the evolution of microbial populations. Genetics 180: 2193-2200.
38. Caraco T, Wang IN, (2008) Free-living pathogens: life-history constraints and strain competition. J Theor Biol 250: 569-579.
39. Walther BA, Ewald PW, (2004) Pathogen survival in the external environment and the evolution of virulence. Biol Rev Camb Philos Soc 79: 849-869.
40. Paepe MD, Taddei F, (2006) Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biol 4: e193.
41. Smith AM, Perelson AS, (2011) Influenza a virus infection kinetics: quantitative data and models. Wiley Interdiscip Rev Syst Biol Med 3: 429-445.
42. Beauchemin CAA, Handel A, (2011) A review of mathematical models of influenza A infections within a host or cell culture: lessons learned and challenges ahead. BMC Public Health 11 (Suppl 1):: S7.
43. Bonhoeffer S, Herz AV, Boerlijst MC, Nee S, Nowak MA, et al. (1996) Explaining "linguistic features" of noncoding DNA. Science 271: 14-15.
44. Joh RI, Wang H, Weiss H, Weitz JS, (2009) Dynamics of indirectly transmitted infectious diseases with immunological threshold. Bull Math Biol 71: 845-862.
45. Kamo M, Boots M, (2004) The curse of the pharaoh in space: free-living infectious stages and the evolution of virulence in spatially explicit populations. J Theor Biol 231: 435-441.
46. Li S, Eisenberg JNS, Spicknall IH, Koopman JS, (2009) Dynamics and control of infections transmitted from person to person through the environment. Am J Epidemiol 170: 257-265.
47. Anderson RM, May RM (1991) Infectious Diseases of Humans- Dynamics and Control. Oxford: Oxford Science Publications.
48. Keeling M, Rohani P (2007) Modeling Infectious Diseases in Humans and Animals. Princeton University Press.
49. Heffernan JM, Smith RJ, Wahl LM, (2005) Perspectives on the basic reproductive ratio. J R Soc Interface 2: 281-293.
50. Alexander DJ, (2000) A review of avian influenza in different bird species. Vet Microbiol 74: 3-13.
51. Swayne DE, editor (2008) Avian Influenza, 1st edition. Wiley-Blackwell.
52. Majumdar SK, Brenner FJ, Huffman JE, McLean RG, Panah AI, et al. (2011) Pandemic Influenza Viruses: Science, Surveillance and Public Health. Pennsylvania Academy of Science.
53. Lange A, Ferguson NM, (2009) Antigenic diversity, transmission mechanisms, and the evolution of pathogens. PLoS Comput Biol 5: e1000536.
54. Chen SC, Chio CP, Jou LJ, Liao CM, (2009) Viral kinetics and exhaled droplet size affect indoor transmission dynamics of influenza infection. Indoor Air 19: 401-413.
55. Hall CB, Douglas R Jr, Geiman JM, Meagher MP, (1979) Viral shedding patterns of children with influenza b infection. J Infect Dis 140: 610-613.
56. Spicknall IH, Koopman JS, Nicas M, Pujol JM, Li S, et al. (2010) Informing optimal environmental influenza interventions: how the host, agent, and environment alter dominant routes of transmission. PLoS Comput Biol 6: e1000969.
57. Halloran SK, Wexler AS, Ristenpart WD, (2012) A comprehensive breath plume model for disease transmission via expiratory aerosols. PLoS One 7: e37088.
58. Handel A, Longini IM, Antia R, (2007) Neuraminidase Inhibitor Resistance in Influenza: Assessing the Danger of Its Generation and Spread. PLoS Comput Biol 3: e240.
59. Haas CN, (1983) Estimation of risk due to low doses of microorganisms: a comparison of alternative methodologies. Am J Epidemiol 118: 573-582.
60. Quinn TC, Wawer MJ, Sewankambo N, Serwadda D, Li C, et al. (2000) Viral load and heterosexual transmission of human immunodeficiency virus type 1. rakai project study group. N Engl J Med 342: 921-929.
61. Hollingsworth TD, Anderson RM, Fraser C, (2008) Hiv-1 transmission, by stage of infection. J Infect Dis 198: 687-693.
62. Ben-Ami F, Regoes RR, Ebert D, (2008) A quantitative test of the relationship between parasite dose and infection probability across different host-parasite combinations. Proc Biol Sci 275: 853-859.
63. Ssematimba A, Hagenaars TJ, de Jong MCM, (2012) Modelling the wind-borne spread of highly pathogenic avian influenza virus between farms. PLoS One 7: e31114.
64. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. ISBN 3-900051-07-0.
65. Marais M, Gugushe N, Maloney SK, Gray DA, (2011) Body temperature responses of pekin ducks (anas platyrhynchos domesticus) exposed to different pathogens. Poult Sci 90: 1234-1238.
66. Throsby M, van den Brink E, Jongeneelen M, Poon LLM, Alard P, et al. (2008) Heterosubtypic neutralizing monoclonal antibodies cross-protective against h5n1 and h1n1 recovered from human igm+ memory b cells. PLoS One 3: e3942.
67. Russell RJ, Kerry PS, Stevens DJ, Steinhauer DA, Martin SR, et al. (2008) Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc Natl Acad Sci U S A 105: 17736-17741.
68. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, et al. (2011) A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza a hemagglutinins. Science 333: 850-856.
69. Brown JD, Berghaus RD, Costa TP, Poulson R, Carter DL, et al. (2012) Intestinal excretion of a wild bird-origin h3n8 low pathogenic avian influenza virus in mallards (anas platyrhynchos). J Wildl Dis 48: 991-998.
70. Smith AM, Adler FR, Perelson AS, (2010) An accurate two-phase approximate solution to an acute viral infection model. J Math Biol 60: 711-726.
71. Uni Z, Ganot S, Sklan D, (1998) Posthatch development of mucosal function in the broiler small intestine. Poult Sci 77: 75-82.
72. Baccam P, Beauchemin C, Macken CA, Hayden FG, Perelson AS, (2006) Kinetics of influenza A virus infection in humans. J Virol 80: 7590-7599.
73. Lee HY, Topham DJ, Park SY, Hollenbaugh J, Treanor J, et al. (2009) Simulation and prediction of the adaptive immune response to influenza a virus infection. J Virol 83: 7151-7165.
74. Saenz RA, Quinlivan M, Elton D, Macrae S, Blunden AS, et al. (2010) Dynamics of influenza virus infection and pathology. J Virol 84: 3974-3983.
75. Handel A, Longini IM, Antia R, (2010) Towards a quantitative understanding of the within-host dynamics of influenza A infections. J R Soc Interface 7: 35-47.
76. Miao H, Hollenbaugh JA, Zand MS, Holden-Wiltse J, Mosmann TR, et al. (2010) Quantifying the early immune response and adaptive immune response kinetics in mice infected with influenza a virus. J Virol 84: 6687-6698.
77. Pawelek KA, Huynh GT, Quinlivan M, Cullinane A, Rong L, et al. (2012) Modeling within-host dynamics of influenza virus infection including immune responses. PLoS Comput Biol 8: e1002588.
78. Coombs D, Gilchrist MA, Ball CL, (2007) Evaluating the importance of within- and between-host selection pressures on the evolution of chronic pathogens. Theor Popul Biol 72: 576-591.
79. Gilchrist MA, Coombs D, (2006) Evolution of virulence: interdependence, constraints, and selection using nested models. Theor Popul Biol 69: 145-153.
80. Luciani F, Sisson SA, Jiang H, Francis AR, Tanaka MM, (2009) The epidemiological fitness cost of drug resistance in mycobacterium tuberculosis. Proc Natl Acad Sci U S A 106: 14711-14715.
81. Day T, Alizon S, Mideo N, (2011) Bridging scales in the evolution of infectious disease life histories: theory. Evolution 65: 3448-3461.
82. Mideo N, Savill NJ, Chadwick W, Schneider P, Read AF, et al. (2011) Causes of variation in malaria infection dynamics: insights from theory and data. Am Nat 178: E174-E188.
83. Read JM, Keeling MJ, (2006) Disease evolution across a range of spatio-temporal scales. Theor Popul Biol 70: 201-213.
84. King AA, Shrestha S, Harvill ET, Bjrnstad ON, (2009) Evolution of acute infections and the invasion-persistence trade-off. Am Nat 173: 446-455.
85. Klinkenberg D, Heesterbeek JAP, (2007) A model for the dynamics of a protozoan parasite within and between successive host populations. Parasitology 134: 949-958.
86. Pepin KM, Volkov I, Banavar JR, Wilke CO, Grenfell BT, (2010) Phenotypic differences in viral immune escape explained by linking within-host dynamics to host-population immunity. J Theor Biol 265: 501-510.
87. Steinmeyer SH, Wilke CO, Pepin KM, (2010) Methods of modelling viral disease dynamics across the within- and between-host scales: The impact of virus dose on host population immunity. Philos Trans R Soc Lond B Biol Sci 365: 1931-1941.
88. Volkov I, Pepin KM, Lloyd-Smith JO, Banavar JR, Grenfell BT, (2010) Synthesizing within-host and population-level selective pressures on viral populations: the impact of adaptive immunity on viral immune escape. J R Soc Interface 7: 1311-1318.
89. Bolker BM (2008) Ecological Models and Data in R. Princeton University Press.