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Pre-symptomatic Influenza Transmission, Surveillance, and School Closings: Implications for Novel Influenza A (H1N1)

Published online by Cambridge University Press:  28 April 2010

G. F. Webb*
Affiliation:
Department of Mathematics, Vanderbilt University, Nashville, Tennessee, 37240 USA
Y-H. Hsieh
Affiliation:
Department of Public Health and Center for Infectious Disease Epidemiology Research, China Medical University, Taichung, Taiwan
J. Wu
Affiliation:
Laboratory for Industrial and Applied Mathematics, Centre for Disease Modeling, Department of Mathematics and Statistics, York University, Toronto, Canada M3J 1P3
M. J. Blaser
Affiliation:
Department of Medicine and Department of Microbiology, New York University School of Medicine, New York, NY 10016, USA
*
*Corresponding author. E-mail glenn.f.webb@vanderbilt.edu
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Abstract

Early studies of the novel swine-origin 2009 influenza A (H1N1) epidemic indicate clinical attack rates in children much higher than in adults. Non-medical interventions such as school closings are constrained by their large socio-economic costs. Here we develop a mathematical model to ascertain the roles of pre-symptomatic influenza transmission as well as symptoms surveillance of children to assess the utility of school closures. Our model analysis indicates that school closings are advisable when pre-symptomatic transmission is significant or when removal of symptomatic children is inefficient. Our objective is to provide a rational basis for school closings decisions dependent on virulence characteristics and local surveillance implementation, applicable to the current epidemic and future epidemics.

Type
Research Article
Copyright
© EDP Sciences, 2010

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References

Arino, J., Brauer, F., van den Driessche, P., Watmough, J. Wu, J.. Simple models for containment of a pandemic . J. R. Soc. Interface, 3 (2006), 453457.CrossRefGoogle ScholarPubMed
Bell, D.M.. World Health Organization Writing Group. Nonpharmaceutical interventions for pandemic influenza, international measures . Emerg. Infect. Dis., 14 (2008), No. 7, 10241030.Google Scholar
Brauer, F.. Age of infection in epidemiology models . Elect. J. Dif. Eqs., 12 (2005), 2937.Google Scholar
Cauchemez, S., Valleron, A.J., Boelle, P.Y., Flahault, A. Ferguson, N.M.. Estimating the impact of school closure on influenza transmission from sentinel data . Nature, 452 (2008), 750754.CrossRefGoogle ScholarPubMed
Carrat, F., Vergu, E., Feguson, N.M., Lemaitre, M., Cauchemez, S., Leach, S. Valleron, A-J.. Time Lines of Infection and Disease in Human Influenza: A Review of Volunteer Challenge Studies . Am. J. Epid., 167 (2008), No. 7, 775785.CrossRefGoogle ScholarPubMed
Chowell, G., Ammon, C.E., Hengartner, N.W. Hyman, J.M.. Estimation of the Reproductive number of the Spanish Flu Epidemic in Geneva, Switzerland . Vaccine, 24 (2006), 67476750.CrossRefGoogle ScholarPubMed
Cowling, B.J., Lau, E.H.Y., Lam, C.L.H., Cheng, C.K.Y., Kovar, J., Chan, K.H., Malik Peiris, J.S., Leung, G.M.. Effects of school closures, 2008 winter influenza season, Hong Kong . Emerg. Infect. Dis., 11 (2006), No. 1, 8187. Google Scholar
Dushoff, J., Plotkin, J.B., Levin, S. Earn, D.J.D.. Dynamical resonance can account for seasonality of influenza epidemics . Proc. Natl. Acad. Sci. USA, 101 (2004), No. 48, 1691516916.CrossRefGoogle ScholarPubMed
Flahault, A., Letrait, S., Blin, P., Hazout, S., Menares, J. Valleron, A.J.. Modeling the 1985 influenza epidemic in France . Stat. Med., 7 (1988), 11471155.CrossRefGoogle Scholar
Feng, Z., Huang, W. Castillo-Chavez, C.. Global behavior of a multi-group SIS epidemic model with age structure . J. Dif. Eq., 218 (2005), 292324.CrossRefGoogle Scholar
Flahault, A., Letrait, S., Blin, P., Hazout, S., Menares, J. Valleron, A.J.. Modeling the 1985 influenza epidemic in France . Stat. Med., 7 (1988), 11471155.CrossRefGoogle Scholar
Frank, A.L., Taber, L.H., Wells, C.R., Wells, J.M., Glezen, W.P. Paredes, A.. Patterns of shedding of myxoviruses and paramyxoviruses in children . J. Infect. Dis., 144 (1981), 433441.CrossRefGoogle ScholarPubMed
Fraser, C., Riley, S., Anderson, R.M. Ferguson, N.M.. Factors that make an infectious disease outbreak controllable , Proc. Natl. Acad. Sci. USA, 101 (2004), No. 16, 61466151.CrossRefGoogle ScholarPubMed
C. Fraser, C.A. Donnelly, S. Cauchemez, W.P. Hanage, M.D. VanKerkhove, T.D. Hollingsworth, J. Griffin, R.F. Baggaley, H.E. Jenkins, E.J. Lyons, T. Jombart, W.R. Hinsley, N.C. Grassly, F. Balloux, A.C. Ghani, N.M. Ferguson, A. Rambaut, O.G. Pybus, H. Lopez-Gatell, C.M Alpuche-Aranda, L.B. Chapela, E.P. Zavala, D.M. Espejo Guevara, F. Checchi, E. Garcia, S. Hugonnet, C. Roth. Pandemic Potential of a Strain of Influenza A (H1N1): Early Findings. Science, published online May 11, 2009.
Gani, R., Hughes, H., Fleming, D., Griffin, T., Medlock, J. Leach, S.. Potential impact of antiviral drug use during influenza pandemic . Emerg. Infect. Dis., 11 (2005), 13551362.CrossRefGoogle Scholar
Germann, T.C., Kadau, K., Longini, I.M. Macken, C.A.. Mitigation strategies for pandemic influenza in the United States . Proc. Natl. Acad. Sci. USA, 103 (2006), 59355940.CrossRefGoogle ScholarPubMed
Graat, J.M., Schouten, E.G., Heijnen, M.-L.A., Kok, F..J., Pallast, E.G.M., deGreeff, S.C. Dorigo-Zetsma, J.W.. A prospective, community-based study on virologic assessment among elderly people with and without symptoms of acute respiratory infection . J. Clin. Epidemiol., 56 (2003), No. 12, 12181223.CrossRefGoogle ScholarPubMed
Hall, C.B., Douglas, R.G. Jr., Geiman, J.M. Meagher, M.P. Viral shedding patterns of children with influenza B infection . J. Infect. Dis., 140 (1979), 610613.CrossRefGoogle ScholarPubMed
Hayden, F.G., Fritz, R.Scott., Lobo, M.C., Alvord, W.G., Strober, W. Straus, S.E.. Local and systemic cytokine responses during experimental human influenza A virus infection. Relation to symptom formation and host defense . J. Clin. Invest., 101 (1998), 643649.CrossRefGoogle ScholarPubMed
H.W. Hethcote. A thousand and one epidemic models. Frontiers in Mathematical Biology, Lecture Notes in Biomathematics 100, S.A. Levin, ed., Springer-Verlag (1994), 504–515.
L.M. Howe. Could the new swine virus be a Òherald waveÓ? Earthfiles.com Environment, published online. Accessed June 1, 2009.
Hsu, S.B. Hsieh, Y.H.. On the Role of Asymptomatic Infection in Transmission Dynamics of Infectious Diseases . Bull. Math. Biol., 70 (2008), 134155.CrossRefGoogle ScholarPubMed
Inaba, H..Nishiura, H.. The basic reproduction number of an infectious disease in a stable population: The impact of population growth rate on the eradication threshold . Math. Model. Nat. Phen., 3 (2008), No. 7, 194228.CrossRefGoogle Scholar
Inaba, H..Nishiura, H.. The state-reproduction number for a multistate class age structured epidemic system and its application to the asymptomatic transmission model . Math. Biosci., 216 (2008), 7789.CrossRefGoogle ScholarPubMed
Johnson, A.J., Moore, Z.S., Edelson, P.J., Kinnane, L., Davies, M., Shay, D.K., Balish, A., McCarron, M., Blanton, L., Finelli, L., Averhoff, F., Bresee, J., Engel, J. Fiore, A.. Household responses to school closure resulting from outbreak of influenza B, North Carolina. BNET: Health Care Industry . Emerg. Infect. Dis., 14 (2008), No. 7, 10241030.CrossRefGoogle Scholar
Kermack, W.O. McKendrick, A.G.. A contribution to the mathematical theory of epidemics . Proc. Roy. Soc. London, 115 (1927), 700721.CrossRefGoogle Scholar
Lessler, J., Cummings, D.A., Fishman, S., Vora, A. Burke, D.S.. Transmissibility of swine flu at Fort Dix, 1976 . J. Roy. Soc. Interface, 4 (2007), No. 15, 55762.CrossRefGoogle ScholarPubMed
Longini, I.M., Halloran, M.E., Nizam, A. Yang, Y. Containing pandemic influenza with antiviral agents . Am. J. Epidemiol., 159 (2004), 623633.CrossRefGoogle ScholarPubMed
Longini, I.M. Jr., Nizam, A., Xu, S., Ungschusak, K., Hanshaoworakul, W., Cummings, D.A.T. Halloran, M.E.. Containing pandemic influenza at the source . Science, 309 (2005), 10831087.CrossRefGoogle ScholarPubMed
Macfarlane, J.T. Lim, W.S.. Bird flu and pandemic flu . British Medical Journal., 331 (2005), 975976.CrossRefGoogle ScholarPubMed
Mills, C.E., Robins, J.M., Lipsitch, M.. Transmissibility of 1918 pandemic influenza . Nature 432, (2004), 904906. CrossRefGoogle ScholarPubMed
Milne, G.J., Kelso, J.K., Kelly, H.A., Huband, S.T., McVernon, J.. A small community model for the transmission of infectious diseases: comparison of school closure as an intervention in individual-based models of an influenza pandemic . PLoSONE, 3 (2008) No. 12, e4005. CrossRefGoogle Scholar
Mniszewski, S.M., Del Valle, S.Y., Stroud, P.D., Riese, J.M. Sydoriak, S.J.. Pandemic simulation of antivirals + school closures: buying time until strain-specific vaccine is available . Comp. & Math. Organ. Theory 14 (2008), No. 3, 209221.CrossRefGoogle Scholar
Monto, A.S., Gunn, R.A., Bandyk, M.G. King, C.L.. Prevention of Russian influenza by amantadine . JAMA, 241 (1979), 10031007.CrossRefGoogle ScholarPubMed
Nafta I, I., Turcanu, A.G., Braun, I., Companetz, W., Simionescu, A., Birt, E. Florea, V.. Administration of amantadine for the prevention of Hong Kong influenza . Bull. World Health Organ., 42 (1970), 423427.Google ScholarPubMed
Ndifon, W., Dushoff, J. Levin, S.A.. On the use of hemagglutination-inhibition for influenza surveillance: Surveillance data are predictive of influenza vaccine effectiveness . Vaccine, 27 (2009), No. 18, 24472452.CrossRefGoogle Scholar
H. Nishiura, C. Castillo-Chavez, M. Safan, G. Chowell. Transmission potential of the new influenza A(H1N1) virus and its age-specificity in Japan. Eurosurveillance, 14 (2009), No. 22, Rapid Communications.
Oker-Blom, N., Hovi, T., Leinikki, P., Palosuo, T., Pettersson, R. Suni, J.. Protection of man from natural infection with influenza A2 Hong Kong virus by amantadine: a controlled field trial . Brit. Med. J., 3 (1970), 676678.CrossRefGoogle ScholarPubMed
Pettersson, R.F., Hellstrom, P.-E., Penttinen, K., Pyhala, R., Tokola, O., Vartio, T., Visakorpi, R.. Evaluation of amantadine in the prophylaxis of influenza A (H1N1) virus infection: a controlled field trial among young adults and high-risk patients . J. Infect. Dis., 142 (1980), 377383. CrossRefGoogle ScholarPubMed
Quarles, J.M., Couch, R.B., Cate, T.R. Goswick, C.B.. Comparison of amantadine and rimantadine for prevention of type A (Russian) influenza . Antiviral Res., 1 (1981), 149155.CrossRefGoogle ScholarPubMed
Sadique, M.Z., Adams, E.J. Edmunds, W.J.. Estimating the costs of school closure for mitigating an influenza pandemic . BMC Public Health, 8 (2008), 135.CrossRefGoogle ScholarPubMed
Senpinar-Brunner, N., Eckert, T. Wyss, K.. Acceptance of public health measures by air travelers, Switzerland . Emerg. Infect. Dis. 15 (2009), No. 5, 831832.CrossRefGoogle ScholarPubMed
Sheat, K.. An investigation into an explosive outbreak of influenza-New Plymouth . Communicable Disease New Zealand, 92 (1992), 1819. Google Scholar
Sato, M., Hosoya, M., Kato, K. Suzuki, H.. Viral shedding in children with influenza virus infections treated with neuraminidase inhibitors . Pediatr. Infect. Dis. J., 24 (2005), 931932.CrossRefGoogle ScholarPubMed
Stilianakis, N.I., Perelson, A.S. Hayden, F.G.. Emergence of drug resistance during an influenza epidemic: insights from a mathematical model . J. Infect. Dis., 177 (1998), No. 4, 863873.CrossRefGoogle ScholarPubMed
World Health Organization. Nonpharmaceutical Interventions for Pandemic Influenza, International Measures. Emerg. Infect. Dis. 12 (2006), No 1, 81–87.
Webb, G.F.. An age-dependent epidemic model with spatial diffusion . Arch. Rat. Mech., 75 (1980), 91102.CrossRefGoogle Scholar