Policy Implications of MISMS Influenza Research

MISMS scientists and collaborators specialize in a broad range of infectious disease research, specifically focusing on influenza virus evolutionary patterns, pandemic preparedness, control strategies, transmission dynamics, and disease burden in varying climates.  Their findings have been published in leading peer-reviewed print journals, and also in innovative online journals like PLoS Currents: Influenza.  Many of these findings can be directly translated to influenza control policies at local, national, and international levels.  MISMS’s work on the current H1N1 pandemic specifically focuses on the epidemiologic impact of the current A/H1N1 pandemic and the effectiveness of control efforts designed to address it. 

Analyses of historical H1N1 data have illustrated the various spatial-temporal models used to describe the disease and its early molecular epidemiology, antigenic and genetic characteristics, and evolutionary history.  Along with data collected from Mexico during the early stages of the current pandemic (Spring 2009), this historical data helps to create a timeline for the spread of the disease.  Early indicators abstracted from this timeline are vital in keeping decision-makers vigilant and thus helping to sustain preparedness efforts earlier in a given season.  MISMS’s research is also helping to identify high-risk populations for H1N1, which, contrasted to seasonal influenza, include children, young adults, and pregnant women.  As a result, these findings provide a better understanding of the groups that require priority immunization in the face of limited vaccine supplies.

While the current H1N1 pandemic most clearly illustrates how MISMS research can be translated to policy, our work on pandemic preparedness and seasonal influenza also has policy implications.  MISMS has worked to support robust preparedness planning at all levels.  A basic understanding of historical data from previous pandemics is needed to create accurate awareness messages and effective preparedness planning for potential pandemics in the future.  The face of a potential pandemic changes with each subsequent circulation of a novel strain, which in turn can result in different transmission dynamics by geography.  As a result, a greater adaptability of pandemic preparedness efforts is needed.

While much attention is typically given to pandemic strains of influenza, much attention must be drawn to the global health burden of seasonal influenza, as it is greater than was previously thought.  Of particular interest to MISMS is the difference in impact of seasonal influenza between tropical and temperate climates.  While the study of influenza in tropical climates is growing in scale, much work needs to be done to gain a more comprehensive understanding of the role influenza circulation in the tropics plays in the global circulation and evolution of the disease. 

Scientific publications supported by MISMS

You can also access all influenza publications supported by MISMS at the Fogarty International Center Division of International Epidemiology and Population Studies Bibliography Website by typing "influenza" as a keyword.
 

Influenza virus evolutionary patterns

1. Lemey P, Suchard M, Rambaut A (Sep 2009) Reconstructing the initial global spread of a human influenza pandemic: A Bayesian spatial-temporal model for the global spread of H1N1pdm. PLoS Currents Influenza. RRN1031.
2. Holmes E (Sep 2009) RNA virus genomics: a world of possibilities. J Clin Invest. 119(9): 2488.
3. Ghedin E, Fitch A, Boyne A, Griesemer S, DePasse J, Bera J, Zhang X, Halpin R, Smit M, Jennings L, St. George K, Holmes EC, Spiro D (Sep 2009) Mixed infection and the genesis of influenza virus diversity. J Virol. 83(17): 8832-41.
4. Rambaut A, Holmes E (Aug 2009) The early molecular epidemiology of the swine-origin A/H1N1 human influenza pandemic. PLoS Currents Influenza. RRN1003.
5. Bahl J, Vijaykrishna D, Holmes EC, Smith GJ, Guan Y (Aug 2009) Gene flow and competitive exclusion of avian influenza A virus in natural reservoir hosts. Virology. 390(2): 289-97.
6. Garten R, Davis C, Russell C, Shu B, Lindstrom S, Balish A, Sessions W, Xu X, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith C, Emery S, Hillman M, Rivailler P, Smagala J, Miranda de Graaf, Burke D, Fouchier R, Pappas C, Alpuche-Aranda C, López-Gatell H, Olivera H, López I, Myers C, Faix D, Blair P, Yu C, Keene K, Dotson PD, Boxrud D, Sambol A, Abid S, St. George K, Bannerman T, Moore A, Stringer D, Blevins P, Demmler-Harrison G, Ginsberg M, Kriner P, Waterman S, Smole S, Guevara H, Belongia E, Clark P, Beatrice S, Donis R, Katz J, Finelli L, Bridges C, Shaw M, Jernigan D, Uyeki T, Smith D, Klimov A, Cox N (Jul 2009) Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science. 325(5937):197-201.
7. Bryant NA, Rash AS, Russell C, Ross J, Cooke A, Bowman S, MacRae S, Lewis N, Paillot R, Zanoni R, Meier H, Griffiths L, Daly J, Tiwari A, Chambers T, Newton J, Elton D (Jul 2009) Antigenic and genetic variations in European and North American equine influenza virus strains (H3N8) isolated from 2006 to 2007. Vet Microbiol. 138(1-2): 41-52.
8. Dunham E, Dugan V, Kaser E, Perkins S, Brown I, Holmes EC, Taubenberger JK (Jun 2009) Different Evolutionary Trajectories of European Avian-Like and Classical Swine H1N1 Influenza A Viruses. J Virol. 83: 5485-94.
9. Nelson MI, Simonsen L, Viboud C, Miller MA, Holmes EC (Jul 2009) The origin and global emergence of adamantane resistant A/H3N2 influenza viruses. Virology. 388(2): 270-8.
10. Chen R, Holmes EC (Jan 2009) Frequent inter-species transmission and geographic subdivision in avian influenza viruses from wild birds. Virology. 383(1): 156-61.
11. Cattoli G, Monne I, Fusaro A, Joannis TM, Lombin LH, Aly MM, Arafa AS, Sturm-Ramirez KM, Couacy-Hymann E, Awuni JA, Batawui KB, Awoume KA, Aplogan GL, Sow A, Ngangnou AC, El Nasri Hamza IM, Gamatié D, Dauphin G, Domenech JM, Capua I (Mar 2009) Highly pathogenic avian influenza virus subtype H5N1 in Africa: a comprehensive phylogenetic analysis and molecular characterization of isolates. PLoS ONE. 4(3): e4842.
12. Nelson MI, Edelman L, Spiro DJ, Boyne AR, Bera J, Halpin R, Ghedin E, Miller MA, Simonsen L, Viboud C, Holmes EC (Aug 2008) Molecular epidemiology of A/H3N2 and A/H1N1 influenza virus during a single epidemic season in the United States. PLoS Pathog. 4(8):e1000133.
13. Chen R, Holmes EC (Jun 2008) The evolutionary dynamics of human influenza B virus. J Mol Evol. 66(6): 655-63.
14. Dugan VG, Chen R, Spiro DJ, Sengamalay N, Zaborsky J, Ghedin E, Nolting J, Swayne DE, Runstadler JA, Happ GM, Senne DA, Wang R, Slemons RD, Holmes EC, Taubenberger JK (May 2008) The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog. 4(5): e1000076.
15. Boni MF, Zhou Y, Taubenberger JK, Holmes EC (May 2008) Homologous recombination is very rare or absent in human influenza A virus. J Virol. 82(10): 4807-11.
16. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC (May 2008) The genomic and epidemiological dynamics of human influenza A virus. Nature. 453(7195): 615–9.
    
17. Duffy S, Shackleton LA, Holmes EC (Apr 2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet. 9(4):267-76.
    
18. Pardini MI, Jamal LF, Durigon EL, Massad E, Perez JF, Pinho JR, Holmes EC, de Andrade Zanotto PM (Mar 2008) Boosting virology in Brazil. PLoS Biology. 6(3):e57.
    
19. Nelson MI, Viboud C, Simonsen L, Bennett RT, Griesemer SB, St George K, Taylor J, Spiro DJ, Sengamalay NA, Ghedin E, Taubenberger JK, Holmes EC (Feb 2008) Multiple reassortment events in the evolutionary history of H1N1 influenza A virus since 1918. PLoS Pathog. 4(2): e1000012.
    
20. Holmes EC (Oct 2007) Viral evolution in the genomic age. PLoS Biol. 5(10): e278.
21. Nelson MI, Simonsen L, Viboud C, Miller MA, Holmes EC. Phylogenetic analysis reveals the global migration of seasonal influenza A viruses. PLoS Pathog. 2007 Sep 14;3(9):1220-8.
22. Simonsen L, Viboud C, Grenfell B, Dushoff J, Jennings L, Smit M, Macken C, Hata M, Gog J, Miller M, Holmes E (Aug 2007) The genesis and spread of reassortment human influenza A/H3N2 viruses conferring adamantane resistance. Mol Biol Evol. 24(8): 1811-20.
    
23. Nelson MI, Holmes EC. The evolution of epidemic influenza. Nature. 2007 March; 8:196-205.
24. Nelson M, Simonsen L, Viboud C, Miller MA, Taylor J, George K, Griesemer S, Ghedin E, Sengamalay N, Spiro D, Volkov I, Grenfell B, Lipman D, Taubenberger J, Holmes E (Dec 2006) Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus. PLoS Pathog. 2(12): e125.
25. Koelle K, Cobey S, Grenfell B, Pascual M (Dec 2006) Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science. 314(5807):1898-903.
26. Chen R, Holmes EC (Dec 2006) Avian influenza virus exhibits rapid evolutionary dynamics. Mol Biol Evol. 23(12): 2336-41.
27. Wolf YL, Viboud C, Holmes EC, Koonin EV, Lipman DJ (Oct 2006) Long intervals of stasis punctuated by bursts of positive selection in the seasonal evolution of influenza A virus. Biology Direct. 1: 34.
28. Holmes EC, Lipman DJ, Zamarin D, Yewdell JW (Sep 2006) Comment on “Large scale sequence analysis of avian influenza isolates“. Science. 313: 1573b.
    
29. Kuiken T, Holmes EC, McCauley J, Rimmelzwaan GF, Williams CS, Grenfell BT (Apr 2006) Host species barriers to influenza virus infections. Science. 312: 394-7.
    
30. Levin SA, Dushoff J, Plotkin JB (Mar-Apr 2004) Evolution and persistence of influenza A and other diseases. Math. Bioscience, 188:17-28.
    
31. Plotkin JB, Dushoff J (Jun 2003) Codon bias and frequency-dependent selection on the hemagglutinin epitopes of influenza A virus. Proc Natl Acad Sci. 100: 7152-7.
    
32. Earn D, Dushoff J, Levin S (Jul 2002) Ecology and evolution of the flu. Trends Ecol Evol. 17: 334-40.
    
33. Plotkin JB, Dushoff J, Levin SA (Apr 2002). Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proc Natl Acad Sci. 99: 6263-8.
    

1. Miller MA, Viboud C, Simonsen L, Olson D, Russell C (Aug 2009 [revised Sep 2009]) Mortality and morbidity burden associated with A/H1N1pdm influenza virus: Who is likely to be infected, experience clinical symptoms, or die from the H1N1pdm 2009 pandemic virus? Version 2. PLoS Currents Influenza. RRN1013.
2. Chowell G, Bertozzi S, Colchero M, Lopez-Gatell H, Alpuche-Aranda C, Hernandez M, Miller MA (Aug 2009) Severe Respiratory Disease Concurrent with the Circulation of H1N1 Influenza. N Engl J Med. 361: 674-9.
3. Miller MA, Viboud C, Balinska M, Simonsen L (Jun 2009) The signature features of influenza pandemics -- implications for policy. N Engl J Med. 360(25): 2595-8.
4. Richard SA, Sugaya N, Simonsen L, Miller MA, Viboud C (Aug 2008) A comparative study of the 1918-1920 influenza pandemic in Japan, USA and UK: mortality impact and implications for pandemic planning. Epidemiol Infect. 137(8): 1062-72.
   
5. Barry JM, Viboud C, Simonsen L (Nov 2008) Cross-Protection between Successive Waves of the 1918–1919 Influenza Pandemic: Epidemiological Evidence from US Army Camps and from Britain. J Infect Dis. 198(10): 1427-34.
   
6. Chowell G, Bettencourt LM, Johnson N, Alonso WJ, Viboud C (Mar 2008) The 1918-1919 influenza pandemic in England and Wales: spatial patterns in transmissibility and mortality impact. Proc Biol Sci. 275(1634): 501-9.
   
7. Andreasen V, Viboud C, Simonsen L (Jan 2008) Epidemiologic characterization of the 1918 influenza pandemic summer wave in Copenhagen: implications for pandemic control strategies. J Infect Dis. 197(2): 270-8.
   
8. Gottfredsson M, Halldórsson BV, Jónsson S, Kristjánsson M, Kristjánsson K, Kristinsson KG, Löve A, Blöndal T, Viboud C, Thorvaldsson S, Helgason A, Gulcher JR, Stefánsson K, Jónsdóttir I (Jan 2008) Lessons from the past: Familial aggregation analysis of fatal pandemic influenza (Spanish flu) in Iceland in 1918. Proc Natl Acad Sci. 105(4): 1303-8.
   
9. Nuño M, Chowell G, Gumel AB (Jun 2007) Assessing the role of basic control measures, antivirals and vaccine in curtailing pandemic influenza: scenarios for the US, UK and the Netherlands. J R Soc Interface. 4: 505-21.
10. Reichert TA (Nov 2005) Preparing for the next influenza pandemic: lessons from multinational data. Pediatr Infect Dis J. 24(11 Suppl): S228-31.
11. Viboud C, Grais RF, Lafont BA, Miller MA, Simonsen L (July 2005) Multinational impact of the 1968 Hong Kong influenza pandemic: evidence for a smoldering pandemic. J Infect Dis. 192(2): 233-48.
    
12. Simonsen L, Olson DR, Viboud C, Heiman E, Miller MA, Reichert TA (2005) Pandemic influenza and mortality: past evidence and projections for the future. In: Knobler S, Oberholtzer K, eds. Forum on Microbial Threats. Pandemic influenza: Assessing capabilities for prevention and response. Washington, DC: Institute of Medicine, The National Academy of Sciences: 89-114.

Vaccine benefits and influenza control strategies

1. Simonsen L, Viboud C, Taylor RJ, Miller MA, Jackson L (Oct 2009) Influenza vaccination and mortality benefits: new insights, new opportunities. Vaccine. 27(45): 6300-4.
2. Chowell G, Viboud C, Wang X, Bertozzi S, Miller M (Aug 2009) Adaptive vaccination strategies to mitigate pandemic influenza: Mexico as a case study. PLoS Currents Influenza. RRN1004.
3. de Mello WA, de Paiva TM, Ishida MA, Benega MA, Dos Santos MC, Viboud C, Miller MA, Alonso WJ (Apr 2009) The dilemma of influenza vaccine recommendations when applied to the tropics: the Brazilian case examined under alternative scenarios. PLoS ONE. 4(4): e5095.
4. Viboud C, Miller MA (Oct 2008) Health benefits of universal influenza vaccination strategy. PLoS Med. 5(10): e216.
5. Miller MA, Viboud C, Olson DR, Grais RF, Rabaa MA, Simonsen L (Aug 2008) Prioritization of influenza pandemic vaccination to minimize years of life lost. J Infect Dis. 198(3): 305-11.
   
6. Chowell G, Miller MA, Viboud C (Jun 2008) Seasonal influenza in the United States, France, and Australia: transmission and prospects for control. Epidemiol Infect. 136(6): 852-64.
7. Simonsen L, Viboud C, Taylor RJ (Dec 2007) Effectiveness of influenza vaccination. NEJM. 357(26): 2729-30.
8. Simonsen L, Taylor R, Viboud C, Miller M, Jackson L (Oct 2007) Mortality benefits of influenza vaccination in elderly people: an ongoing controversy. Lancet Infect Dis. 7(10): 658-66.
9. Dushoff J, Plotkin JB, Viboud C, Simonsen L, Miller M, Loeb M, Earn DJ (May 2007) Vaccinating to protect a vulnerable subpopulation. PLoS Med 4(5): e174.
10. Le Menach A, Vergu E, Grais RF, Smith DL, Flahault A (Oct 2006) Key strategies for reducing spread of avian influenza among commercial poultry holdings: lessons for transmission to humans. Proc Biol Sci. 273(1600): 2467-75.
    
11. Goodwin K, Viboud C, Simonsen L (Feb 2006) Antibody response to influenza vaccination in the elderly: A quantitative review. Vaccine. 24(8):1159-69.
    
12. Simonsen L, Viboud C, Taylor R (Dec 2005) Influenza vaccination in elderly people. Lancet. 366(9503): 2086.
    
13. Simonsen L, Reichert TA, Viboud C, Blackwelder WC, Taylor RJ, Miller MA (Feb 2005) Impact of influenza vaccination on seasonal mortality in the US elderly population. Archives of Internal Medicine. 165(3): 265-72.
    
14. Simonsen L, Viboud C, Blackwelder WC, Taylor RJ, Miller MA (Aug 2005) Researchers defend influenza vaccine study. Infect Dis News. (Guest Editorial)
15. Reichert TA (Apr 2002) The Japanese program of vaccination of schoolchildren against influenza:implications for control of the disease. Semin Pediatr Infect Dis. 13(2): 104-11.
    
16. Reichert TA, Sugaya, N, Fedson DS, Glezen WP, Simonsen L, Tashiro M (Mar 2001) The Japanese experience with vaccinating school children against influenza. N Engl J Med. 344(12): 889-96.

1. Park AW, Daly JM, Lewis NS, Smith DJ, Wood JL, Grenfell BT (Oct 2009) Quantifying the impact of immune escape on transmission dynamics of influenza. Science. 326(5953): 726-8.
2. Munayco CV, Gómez J, Laguna-Torres VA, Arrasco J, Kochel TJ, Fiestas V, Garcia J, Perez J, Torres I, Condori F, Nishiura H, Chowell G (Aug 2009) Epidemiological and transmissibility analysis of influenza A(H1N1)v in a southern hemisphere setting: Peru. Euro Surveill. 14(32): 1-5.
3. Rivas A, Chowell G, Schwager S, Fasina FO, Hoogesteijn A, Smith SD, Bisschop S, Anderson K, Hyman JM (Aug 2009) Lessons from Nigeria: the role of roads in the geo-temporal progression of avian influenza (H5N1) virus. Epidemiol Infect. 1-7. Epub: 05 Aug 2009.
4. Lipsitch M, Viboud C (Mar 2009) Influenza seasonality: lifting the fog. Proc Natl Acad Sci. 106(10): 3645-6.
5. Finkelman BS, Viboud C, Koelle K, Ferrari MJ, Bharti N, Grenfell BT (Dec 2007) Global patterns in  seasonal activity of influenza A/H3N2, A/H1N1, and B from 1997 to 2005: viral coexistence and latitudinal gradients. PLoS ONE. 2(12): e1296.
6. Alonso WJ, Viboud C, Simonsen L, Hirano EW, Daufenbach LZ, Miller MA (Jun 2007) Seasonality of influenza in Brazil: a traveling wave from the Amazon to the subtropics. Am J Epidemiol. 165(12):1434-42.
7. Viboud C, Tam T, Fleming D, Handel A, Miller M, Simonsen L (Nov 2006) Transmissibility and mortality impact of epidemic and pandemic influenza, with emphasis on the unusually deadly 1951 epidemic. Vaccine. 24(44-46): 6701-7.
8. Viboud C, Miller MA, Grenfell B, Bjørnstad O, Simonsen L (Nov 2006) Air travel and the spread of influenza: important caveats. PLos Med. 3(11): e503.
   
9. Viboud C, Bjørnstad O, Smith DL, Simonsen L, Miller MA, Grenfell B (Apr 2006) Synchrony, waves, and spatial hierarchies in the spread of influenza. Science. 312(5772): 447-51.
10. Viboud C, Boëlle PY, Cauchemez S, Lavenu A, Valleron AJ, Flahault A, Carrat F (Sept 2004) Risk factors of influenza transmission in households. Br J Gen Pract. 54(506): 684-9.
    
11. Cauchemez S, Carrat F, Viboud C, Valleron AJ, Boëlle PY (Nov 2004) A Bayesian MCMC approach to study transmission of influenza: application to household longitudinal data. Stat Med. 23(22): 3469-87.
12. Viboud C, Boëlle P-Y, Pakdaman KP, Carrat F, Valleron A-J, Flahault A (Jan 2004) Influenza epidemics in the USA, France, and Australia, 1972-1997. Emerg Infect Dis. 10(1): 32-9.
    
13. Viboud C, Boëlle P-Y, Carrat F, Valleron A-J, Flahault A (Nov 2003) Prediction of the spread of influenza epidemics by the method of analogues. Am J of Epidemiol. 158:10; 996-1006.
    

Influenza disease burden in the tropics and temperate climates

1. Newall A, Viboud C, Wood J (Nov 2009) Influenza-attributable mortality in Australians aged more than 50 years: a comparison of different modelling approaches. Epidemiol Infect. 2009 Nov 27: 1-7. [Epub ahead of print]
2. Gordon A, Videa E, Saborio S, López R, Kuan G, Reingold A, Balmaseda A, Harris E (Nov 2009) Performance of an influenza rapid test in children in a primary healthcare setting in Nicaragua. PLoS One. 4(11): e7907.
3. Rizzo C, Bella A, Viboud C, Simonsen L, Miller MA, Rota MC, Salmaso S, Ciofi Degli Atti ML (May 2007) Trends for influenza-related deaths during pandemic and epidemic seasons, Italy, 1969-2001. Emerg Infect Dis. 13(5): 694-9.
4. Rizzo C, Viboud C, Montomoli E, Simonsen L, Miller MA (Oct 2006) Influenza-related mortality in the Italian elderly: no decline associated with increasing vaccination coverage. Vaccine. 24(42-43): 6468-75.
5. Viboud C, Tam T, Fleming D, Miller M, Simonsen L (Apr 2006) 1951 influenza epidemic, England and Wales, Canada, and the United States. Emerg Infect Dis. 12(4): 661-8.
6. Viboud C, Alonso WJ, Simonsen L (Mar 2006) Influenza in tropical regions. Plos Med. 3(4): e89.
7. Dushoff J, Plotkin JB, Viboud C, Earn DJ, Simonsen L (Jan 2006) Mortality due to influenza in the United States – an annualized regression approach using multiple-cause mortality data. Am J Epidemiol. 163(2):181-7.
8. Simonsen L, Taylor R, Viboud C, Dushoff J, Miller MA (Jan 2006) US flu mortality estimates are based on solid science. BMJ. 332(7534): 177-8.
9. Dushoff J (Jul 2005) Assessing influenza-related mortality: Comment on Zucs et al. Emerg Themes Epidemiol. 2:7.
   
10. Dushoff J, Plotkin JB, Levin SA, Earn DJ. Dynamical resonance can account for seasonality of influenza epidemics. Proc Natl Acad Sci. 101(48): 16915-6.
    
11. Reichert TA, Simonsen L, Sharma A, Pardo SA, Fedson DS, Miller MA (Sep 2004) Influenza and the winter increase in mortality in the United States, 1959-1999. Am J Epidemiol. 160(5): 492-502.
    
12. Viboud C, Pakdaman K., Boëlle P-Y, Myers M, Wilson ML, Valleron A-J, Flahault A (Nov 2004) Association of influenza epidemics with global climate variability. Eur J Epidemiol. 19(11): 1055-9.
    
13. Simonsen L, Blackwelder WC, Reichert TA, Miller MA (May 2003) Estimating deaths due to influenza and respiratory syncytial virus. JAMA. 289(19): 2499-500.