Skip to main content
Top
Published in: BMC Medicine 1/2006

Open Access 01-12-2006 | Research article

A 'small-world-like' model for comparing interventions aimed at preventing and controlling influenza pandemics

Authors: Fabrice Carrat, Julie Luong, Hervé Lao, Anne-Violaine Sallé, Christian Lajaunie, Hans Wackernagel

Published in: BMC Medicine | Issue 1/2006

Login to get access

Abstract

Background

With an influenza pandemic seemingly imminent, we constructed a model simulating the spread of influenza within the community, in order to test the impact of various interventions.

Methods

The model includes an individual level, in which the risk of influenza virus infection and the dynamics of viral shedding are simulated according to age, treatment, and vaccination status; and a community level, in which meetings between individuals are simulated on randomly generated graphs. We used data on real pandemics to calibrate some parameters of the model. The reference scenario assumes no vaccination, no use of antiviral drugs, and no preexisting herd immunity. We explored the impact of interventions such as vaccination, treatment/prophylaxis with neuraminidase inhibitors, quarantine, and closure of schools or workplaces.

Results

In the reference scenario, 57% of realizations lead to an explosive outbreak, lasting a mean of 82 days (standard deviation (SD) 12 days) and affecting 46.8% of the population on average. Interventions aimed at reducing the number of meetings, combined with measures reducing individual transmissibility, would be partly effective: coverage of 70% of affected households, with treatment of the index patient, prophylaxis of household contacts, and confinement to home of all household members, would reduce the probability of an outbreak by 52%, and the remaining outbreaks would be limited to 17% of the population (range 0.8%–25%). Reactive vaccination of 70% of the susceptible population would significantly reduce the frequency, size, and mean duration of outbreaks, but the benefit would depend markedly on the interval between identification of the first case and the beginning of mass vaccination. The epidemic would affect 4% of the population if vaccination started immediately, 17% if there was a 14-day delay, and 36% if there was a 28-day delay. Closing schools when the number of infections in the community exceeded 50 would be very effective, limiting the size of outbreaks to 10% of the population (range 0.9%–22%).

Conclusion

This flexible tool can help to determine the interventions most likely to contain an influenza pandemic. These results support the stockpiling of antiviral drugs and accelerated vaccine development.
Appendix
Available only for authorised users
Literature
2.
go back to reference Stohr K, Esveld M: Public health. Will vaccines be available for the next influenza pandemic?. Science. 2004, 306: 2195-2196. 10.1126/science.1108165.CrossRefPubMed Stohr K, Esveld M: Public health. Will vaccines be available for the next influenza pandemic?. Science. 2004, 306: 2195-2196. 10.1126/science.1108165.CrossRefPubMed
3.
go back to reference Bresson JL, Perronne C, Launay O, Gerdil C, Saville M, Wood J, Hoschler K, Zambon MC: Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet. 2006, 367: 1657-1664. 10.1016/S0140-6736(06)68656-X.CrossRefPubMed Bresson JL, Perronne C, Launay O, Gerdil C, Saville M, Wood J, Hoschler K, Zambon MC: Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet. 2006, 367: 1657-1664. 10.1016/S0140-6736(06)68656-X.CrossRefPubMed
4.
go back to reference Treanor JJ, Campbell JD, Zangwill KM, Rowe T, Wolff M: Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. N Engl J Med. 2006, 354: 1343-1351. 10.1056/NEJMoa055778.CrossRefPubMed Treanor JJ, Campbell JD, Zangwill KM, Rowe T, Wolff M: Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. N Engl J Med. 2006, 354: 1343-1351. 10.1056/NEJMoa055778.CrossRefPubMed
5.
go back to reference Ferguson NM, Cummings DA, Cauchemez S, Fraser C, Riley S, Meeyai A, Iamsirithaworn S, Burke DS: Strategies for containing an emerging influenza pandemic in Southeast Asia. Nature. 2005, 437: 209-214. 10.1038/nature04017.CrossRefPubMed Ferguson NM, Cummings DA, Cauchemez S, Fraser C, Riley S, Meeyai A, Iamsirithaworn S, Burke DS: Strategies for containing an emerging influenza pandemic in Southeast Asia. Nature. 2005, 437: 209-214. 10.1038/nature04017.CrossRefPubMed
6.
go back to reference Longini IM, Nizam A, Xu S, Ungchusak K, Hanshaoworakul W, Cummings DA, Halloran ME: Containing pandemic influenza at the source. Science. 2005, 309: 1083-1087. 10.1126/science.1115717.CrossRefPubMed Longini IM, Nizam A, Xu S, Ungchusak K, Hanshaoworakul W, Cummings DA, Halloran ME: Containing pandemic influenza at the source. Science. 2005, 309: 1083-1087. 10.1126/science.1115717.CrossRefPubMed
7.
go back to reference Ferguson NM, Cummings DA, Fraser C, Cajka JC, Cooley PC, Burke DS: Strategies for mitigating an influenza pandemic. Nature. 2006, 442: 448-452. 10.1038/nature04795.CrossRefPubMed Ferguson NM, Cummings DA, Fraser C, Cajka JC, Cooley PC, Burke DS: Strategies for mitigating an influenza pandemic. Nature. 2006, 442: 448-452. 10.1038/nature04795.CrossRefPubMed
8.
go back to reference Germann TC, Kadau K, Longini IM, Macken CA: Mitigation strategies for pandemic influenza in the United States. Proc Natl Acad Sci USA. 2006, 103: 5935-5940. 10.1073/pnas.0601266103.CrossRefPubMedPubMedCentral Germann TC, Kadau K, Longini IM, Macken CA: Mitigation strategies for pandemic influenza in the United States. Proc Natl Acad Sci USA. 2006, 103: 5935-5940. 10.1073/pnas.0601266103.CrossRefPubMedPubMedCentral
9.
go back to reference Longini IM, Halloran ME, Nizam A, Yang Y: Containing pandemic influenza with antiviral agents. Am J Epidemiol. 2004, 159: 623-633. 10.1093/aje/kwh092.CrossRefPubMed Longini IM, Halloran ME, Nizam A, Yang Y: Containing pandemic influenza with antiviral agents. Am J Epidemiol. 2004, 159: 623-633. 10.1093/aje/kwh092.CrossRefPubMed
10.
go back to reference Treanor JJ, Hayden F: Volunteer challenge studies. Textbook of Influenza. Edited by: Nicholson KG, Webster RG, Hay AJ. 1998, London: Blackwell Science, 517-537. Treanor JJ, Hayden F: Volunteer challenge studies. Textbook of Influenza. Edited by: Nicholson KG, Webster RG, Hay AJ. 1998, London: Blackwell Science, 517-537.
11.
go back to reference Carrat F, Vergu E, Ferguson NM, Cauchemez S, Leach S, Valleron AJ: Time lines of infection and disease in human influenza [abstract]. 46th Interscience Conference on Antimicrobial Agents and Chemotherapy: 27–30 September 2006; abstract number V-1698. 2006, San Francisco. Washington: American Society of Microbiology, 455. Carrat F, Vergu E, Ferguson NM, Cauchemez S, Leach S, Valleron AJ: Time lines of infection and disease in human influenza [abstract]. 46th Interscience Conference on Antimicrobial Agents and Chemotherapy: 27–30 September 2006; abstract number V-1698. 2006, San Francisco. Washington: American Society of Microbiology, 455.
12.
go back to reference Carrat F, Sahler C, Rogez S, Leruez-Ville M, Freymuth F, Le Gales C, Bungener M, Housset B, Nicolas M, Rouzioux C: Influenza burden of illness: estimates from a national prospective survey of household contacts in France. Arch Intern Med. 2002, 162: 1842-1848. 10.1001/archinte.162.16.1842.CrossRefPubMed Carrat F, Sahler C, Rogez S, Leruez-Ville M, Freymuth F, Le Gales C, Bungener M, Housset B, Nicolas M, Rouzioux C: Influenza burden of illness: estimates from a national prospective survey of household contacts in France. Arch Intern Med. 2002, 162: 1842-1848. 10.1001/archinte.162.16.1842.CrossRefPubMed
13.
go back to reference Cauchemez S, Carrat F, Viboud C, Valleron AJ, Boelle PY: A Bayesian MCMC approach to study transmission of influenza: application to household longitudinal data. Stat Med. 2004, 23: 3469-3487. 10.1002/sim.1912.CrossRefPubMed Cauchemez S, Carrat F, Viboud C, Valleron AJ, Boelle PY: A Bayesian MCMC approach to study transmission of influenza: application to household longitudinal data. Stat Med. 2004, 23: 3469-3487. 10.1002/sim.1912.CrossRefPubMed
14.
go back to reference Viboud C, Boelle PY, Cauchemez S, Lavenu A, Valleron AJ, Flahault A, Carrat F: Risk factors of influenza transmission in households. Br J Gen Pract. 2004, 54: 684-689.PubMedPubMedCentral Viboud C, Boelle PY, Cauchemez S, Lavenu A, Valleron AJ, Flahault A, Carrat F: Risk factors of influenza transmission in households. Br J Gen Pract. 2004, 54: 684-689.PubMedPubMedCentral
15.
go back to reference Calfee DP, Peng AW, Cass LM, Lobo M, Hayden FG: Safety and efficacy of intravenous zanamivir in preventing experimental human influenza A virus infection. Antimicrob Agents Chemother. 1999, 43: 1616-1620.PubMedPubMedCentral Calfee DP, Peng AW, Cass LM, Lobo M, Hayden FG: Safety and efficacy of intravenous zanamivir in preventing experimental human influenza A virus infection. Antimicrob Agents Chemother. 1999, 43: 1616-1620.PubMedPubMedCentral
16.
go back to reference Doyle WJ, Skoner DP, Alper CM, Allen G, Moody SA, Seroky JT, Hayden FG: Effect of rimantadine treatment on clinical manifestations and otologic complications in adults experimentally infected with influenza A (H1N1) virus. J Infect Dis. 1998, 177: 1260-1265.CrossRefPubMed Doyle WJ, Skoner DP, Alper CM, Allen G, Moody SA, Seroky JT, Hayden FG: Effect of rimantadine treatment on clinical manifestations and otologic complications in adults experimentally infected with influenza A (H1N1) virus. J Infect Dis. 1998, 177: 1260-1265.CrossRefPubMed
17.
go back to reference Fritz RS, Hayden FG, Calfee DP, Cass LM, Peng AW, Alvord WG, Strober W, Straus SE: Nasal cytokine and chemokine responses in experimental influenza A virus infection: results of a placebo-controlled trial of intravenous zanamivir treatment. J Infect Dis. 1999, 180: 586-593. 10.1086/314938.CrossRefPubMed Fritz RS, Hayden FG, Calfee DP, Cass LM, Peng AW, Alvord WG, Strober W, Straus SE: Nasal cytokine and chemokine responses in experimental influenza A virus infection: results of a placebo-controlled trial of intravenous zanamivir treatment. J Infect Dis. 1999, 180: 586-593. 10.1086/314938.CrossRefPubMed
18.
go back to reference Hayden FG, Jennings L, Robson R, Schiff G, Jackson H, Rana B, McClelland G, Ipe D, Roberts N, Ward P: Oral oseltamivir in human experimental influenza B infection. Antivir Ther. 2000, 5: 205-213.PubMed Hayden FG, Jennings L, Robson R, Schiff G, Jackson H, Rana B, McClelland G, Ipe D, Roberts N, Ward P: Oral oseltamivir in human experimental influenza B infection. Antivir Ther. 2000, 5: 205-213.PubMed
19.
go back to reference Hayden FG, Treanor JJ, Fritz RS, Lobo M, Betts RF, Miller M, Kinnersley N, Mills RG, Ward P, Straus SE: Use of the oral neuraminidase inhibitor oseltamivir in experimental human influenza: randomized controlled trials for prevention and treatment. JAMA. 1999, 282: 1240-1246. 10.1001/jama.282.13.1240.CrossRefPubMed Hayden FG, Treanor JJ, Fritz RS, Lobo M, Betts RF, Miller M, Kinnersley N, Mills RG, Ward P, Straus SE: Use of the oral neuraminidase inhibitor oseltamivir in experimental human influenza: randomized controlled trials for prevention and treatment. JAMA. 1999, 282: 1240-1246. 10.1001/jama.282.13.1240.CrossRefPubMed
20.
go back to reference Hayden FG, Fritz R, Lobo MC, Alvord W, Strober W, Straus SE: Local and systemic cytokine responses during experimental human influenza A virus infection. Relation to symptom formation and host defense. J Clin Invest. 1998, 101: 643-649.CrossRefPubMedPubMedCentral Hayden FG, Fritz R, Lobo MC, Alvord W, Strober W, Straus SE: Local and systemic cytokine responses during experimental human influenza A virus infection. Relation to symptom formation and host defense. J Clin Invest. 1998, 101: 643-649.CrossRefPubMedPubMedCentral
21.
go back to reference Walker JB, Hussey EK, Treanor JJ, Montalvo A, Hayden FG: Effects of the neuraminidase inhibitor zanamavir on otologic manifestations of experimental human influenza. J Infect Dis. 1997, 176: 1417-1422.CrossRefPubMed Walker JB, Hussey EK, Treanor JJ, Montalvo A, Hayden FG: Effects of the neuraminidase inhibitor zanamavir on otologic manifestations of experimental human influenza. J Infect Dis. 1997, 176: 1417-1422.CrossRefPubMed
26.
go back to reference Barabasi AL, Albert R: Emergence of scaling in random networks. Science. 1999, 286: 509-512. 10.1126/science.286.5439.509.CrossRefPubMed Barabasi AL, Albert R: Emergence of scaling in random networks. Science. 1999, 286: 509-512. 10.1126/science.286.5439.509.CrossRefPubMed
27.
go back to reference Newman M: The structure and function of complex networks. SIAM REVIEW. 2003, 45: 167-256. 10.1137/S003614450342480.CrossRef Newman M: The structure and function of complex networks. SIAM REVIEW. 2003, 45: 167-256. 10.1137/S003614450342480.CrossRef
28.
go back to reference Barabasi A, Albert R, Jeong H: Mean-field theory for scale-free random networks. Physica A. 1999, 272: 173-187. 10.1016/S0378-4371(99)00291-5.CrossRef Barabasi A, Albert R, Jeong H: Mean-field theory for scale-free random networks. Physica A. 1999, 272: 173-187. 10.1016/S0378-4371(99)00291-5.CrossRef
29.
go back to reference Watts DJ, Strogatz SH: Collective dynamics of 'small-world' networks. Nature. 1998, 393: 440-442. 10.1038/30918.CrossRefPubMed Watts DJ, Strogatz SH: Collective dynamics of 'small-world' networks. Nature. 1998, 393: 440-442. 10.1038/30918.CrossRefPubMed
30.
go back to reference Andersson H: Limit theorems for a random graph epidemic model. Ann Appl Prob. 1998, 8: 1331-1349. 10.1214/aoap/1028903384.CrossRef Andersson H: Limit theorems for a random graph epidemic model. Ann Appl Prob. 1998, 8: 1331-1349. 10.1214/aoap/1028903384.CrossRef
31.
go back to reference Jordan WS, Denny FW, Badger GF, Curtiss C, Dingle JH, Oseasohn R, Stevens DA: A study of illness in a group of Cleveland families. XVII. The occurrence of Asian influenza. Am J Hyg. 1958, 68: 190-212.PubMed Jordan WS, Denny FW, Badger GF, Curtiss C, Dingle JH, Oseasohn R, Stevens DA: A study of illness in a group of Cleveland families. XVII. The occurrence of Asian influenza. Am J Hyg. 1958, 68: 190-212.PubMed
32.
go back to reference Mills CE, Robins JM, Lipsitch M: Transmissibility of 1918 pandemic influenza. Nature. 2004, 432: 904-906. 10.1038/nature03063.CrossRefPubMed Mills CE, Robins JM, Lipsitch M: Transmissibility of 1918 pandemic influenza. Nature. 2004, 432: 904-906. 10.1038/nature03063.CrossRefPubMed
33.
go back to reference Simonsen L, Clarke MJ, Schonberger LB, Arden NH, Cox NJ, Fukuda K: Pandemic versus epidemic influenza mortality: a pattern of changing age distribution. J Infect Dis. 1998, 178: 53-60.CrossRefPubMed Simonsen L, Clarke MJ, Schonberger LB, Arden NH, Cox NJ, Fukuda K: Pandemic versus epidemic influenza mortality: a pattern of changing age distribution. J Infect Dis. 1998, 178: 53-60.CrossRefPubMed
34.
go back to reference Moscona A: Neuraminidase inhibitors for influenza. N Engl J Med. 2005, 353: 1363-1373. 10.1056/NEJMra050740.CrossRefPubMed Moscona A: Neuraminidase inhibitors for influenza. N Engl J Med. 2005, 353: 1363-1373. 10.1056/NEJMra050740.CrossRefPubMed
35.
go back to reference Cooper NJ, Sutton AJ, Abrams KR, Wailoo A, Turner D, Nicholson KG: Effectiveness of neuraminidase inhibitors in treatment and prevention of influenza A and B: systematic review and meta-analyses of randomised controlled trials. BMJ. 2003, 326: 1235-10.1136/bmj.326.7401.1235.CrossRefPubMedPubMedCentral Cooper NJ, Sutton AJ, Abrams KR, Wailoo A, Turner D, Nicholson KG: Effectiveness of neuraminidase inhibitors in treatment and prevention of influenza A and B: systematic review and meta-analyses of randomised controlled trials. BMJ. 2003, 326: 1235-10.1136/bmj.326.7401.1235.CrossRefPubMedPubMedCentral
36.
go back to reference Hayden FG, Belshe R, Villanueva C, Lanno R, Hughes C, Small I, Dutkowski R, Ward P, Carr J: Management of influenza in households: a prospective, randomized comparison of oseltamivir treatment with or without postexposure prophylaxis. J Infect Dis. 2004, 189: 440-449. 10.1086/381128.CrossRefPubMed Hayden FG, Belshe R, Villanueva C, Lanno R, Hughes C, Small I, Dutkowski R, Ward P, Carr J: Management of influenza in households: a prospective, randomized comparison of oseltamivir treatment with or without postexposure prophylaxis. J Infect Dis. 2004, 189: 440-449. 10.1086/381128.CrossRefPubMed
37.
go back to reference Smith PG, Rodrigues LC, Fine PE: Assessment of the protective efficacy of vaccines against common diseases using case-control and cohort studies. Int J Epidemiol. 1984, 13: 87-93.CrossRefPubMed Smith PG, Rodrigues LC, Fine PE: Assessment of the protective efficacy of vaccines against common diseases using case-control and cohort studies. Int J Epidemiol. 1984, 13: 87-93.CrossRefPubMed
38.
go back to reference Nichol KL, Lind A, Margolis KL, Murdoch M, McFadden R, Hauge M, Magnan S, Drake M: The effectiveness of vaccination against influenza in healthy, working adults. N Engl J Med. 1995, 333: 889-893. 10.1056/NEJM199510053331401.CrossRefPubMed Nichol KL, Lind A, Margolis KL, Murdoch M, McFadden R, Hauge M, Magnan S, Drake M: The effectiveness of vaccination against influenza in healthy, working adults. N Engl J Med. 1995, 333: 889-893. 10.1056/NEJM199510053331401.CrossRefPubMed
39.
go back to reference Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM: Superspreading and the effect of individual variation on disease emergence. Nature. 2005, 438: 355-359. 10.1038/nature04153.CrossRefPubMed Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM: Superspreading and the effect of individual variation on disease emergence. Nature. 2005, 438: 355-359. 10.1038/nature04153.CrossRefPubMed
40.
go back to reference Newman ME: Properties of highly clustered networks. Phys Rev E Stat Nonlin Soft Matter Phys. 2003, 68: 026121.CrossRefPubMed Newman ME: Properties of highly clustered networks. Phys Rev E Stat Nonlin Soft Matter Phys. 2003, 68: 026121.CrossRefPubMed
41.
go back to reference Antia R, Regoes RR, Koella JC, Bergstrom CT: The role of evolution in the emergence of infectious diseases. Nature. 2003, 426: 658-661. 10.1038/nature02104.CrossRefPubMed Antia R, Regoes RR, Koella JC, Bergstrom CT: The role of evolution in the emergence of infectious diseases. Nature. 2003, 426: 658-661. 10.1038/nature02104.CrossRefPubMed
42.
go back to reference Drake JM: Limits to forecasting precision for outbreaks of directly transmitted diseases. PLoS Med. 2006, 3: e3-10.1371/journal.pmed.0030003.CrossRefPubMed Drake JM: Limits to forecasting precision for outbreaks of directly transmitted diseases. PLoS Med. 2006, 3: e3-10.1371/journal.pmed.0030003.CrossRefPubMed
43.
go back to reference Kiso M, Mitamura K, Sakai-Tagawa Y, Shiraishi K, Kawakami C, Kimura K, Hayden FG, Sugaya N, Kawaoka Y: Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet. 2004, 364: 759-765. 10.1016/S0140-6736(04)16934-1.CrossRefPubMed Kiso M, Mitamura K, Sakai-Tagawa Y, Shiraishi K, Kawakami C, Kimura K, Hayden FG, Sugaya N, Kawaoka Y: Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet. 2004, 364: 759-765. 10.1016/S0140-6736(04)16934-1.CrossRefPubMed
44.
go back to reference Le QM, Kiso M, Someya K, Sakai YT, Nguyen TH, Nguyen KH, Pham ND, Ngyen HH, Yamada S, Muramoto Y, Horimoto T, Takada A, Goto H, Suzuki T, Suzuki Y, Kawaoka Y: Avian flu: isolation of drug-resistant H5N1 virus. Nature. 2005, 437: 1108-10.1038/4371108a.CrossRefPubMed Le QM, Kiso M, Someya K, Sakai YT, Nguyen TH, Nguyen KH, Pham ND, Ngyen HH, Yamada S, Muramoto Y, Horimoto T, Takada A, Goto H, Suzuki T, Suzuki Y, Kawaoka Y: Avian flu: isolation of drug-resistant H5N1 virus. Nature. 2005, 437: 1108-10.1038/4371108a.CrossRefPubMed
45.
go back to reference Eubank S, Guclu H, Kumar VS, Marathe MV, Srinivasan A, Toroczkai Z, Wang N: Modelling disease outbreaks in realistic urban social networks. Nature. 2004, 429: 180-184. 10.1038/nature02541.CrossRefPubMed Eubank S, Guclu H, Kumar VS, Marathe MV, Srinivasan A, Toroczkai Z, Wang N: Modelling disease outbreaks in realistic urban social networks. Nature. 2004, 429: 180-184. 10.1038/nature02541.CrossRefPubMed
46.
go back to reference Galvani AP, May RM: Epidemiology: dimensions of superspreading. Nature. 2005, 438: 293-295. 10.1038/438293a.CrossRefPubMed Galvani AP, May RM: Epidemiology: dimensions of superspreading. Nature. 2005, 438: 293-295. 10.1038/438293a.CrossRefPubMed
47.
go back to reference Woolhouse ME, Dye C, Etard JF, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JL, Ndhlovu PD, Quinnell RJ, Watts CH, Chandiwana SK, Anderson RM: Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci USA. 1997, 94: 338-342. 10.1073/pnas.94.1.338.CrossRefPubMedPubMedCentral Woolhouse ME, Dye C, Etard JF, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JL, Ndhlovu PD, Quinnell RJ, Watts CH, Chandiwana SK, Anderson RM: Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci USA. 1997, 94: 338-342. 10.1073/pnas.94.1.338.CrossRefPubMedPubMedCentral
48.
go back to reference Frank AL, Taber LH, Wells JM: Comparison of infection rates and severity of illness for influenza A subtypes H1N1 and H3N2. J Infect Dis. 1985, 151: 73-80.CrossRefPubMed Frank AL, Taber LH, Wells JM: Comparison of infection rates and severity of illness for influenza A subtypes H1N1 and H3N2. J Infect Dis. 1985, 151: 73-80.CrossRefPubMed
49.
go back to reference Axtell RL: Zipf distribution of U.S. firm sizes. Science. 2001, 293: 1818-1820. 10.1126/science.1062081.CrossRefPubMed Axtell RL: Zipf distribution of U.S. firm sizes. Science. 2001, 293: 1818-1820. 10.1126/science.1062081.CrossRefPubMed
Metadata
Title
A 'small-world-like' model for comparing interventions aimed at preventing and controlling influenza pandemics
Authors
Fabrice Carrat
Julie Luong
Hervé Lao
Anne-Violaine Sallé
Christian Lajaunie
Hans Wackernagel
Publication date
01-12-2006
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2006
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/1741-7015-4-26

Other articles of this Issue 1/2006

BMC Medicine 1/2006 Go to the issue