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Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Direct and indirect effects of influenza vaccination

Authors: Martin Eichner, Markus Schwehm, Linda Eichner, Laetitia Gerlier

Published in: BMC Infectious Diseases | Issue 1/2017

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Abstract

Background

After vaccination, vaccinees acquire some protection against infection and/or disease. Vaccination, therefore, reduces the number of infections in the population. Due to this herd protection, not everybody needs to be vaccinated to prevent infections from spreading.

Methods

We quantify direct and indirect effects of influenza vaccination examining the standard Susceptible-Infected-Recovered (SIR) and Susceptible-Infected-Recovered-Susceptible (SIRS) model as well as simulation results of a sophisticated simulation tool which allows for seasonal transmission of four influenza strains in a population with realistic demography and age-dependent contact patterns.

Results

As shown analytically for the simple SIR and SIRS transmission models, indirect vaccination effects are bigger than direct ones if the effective reproduction number of disease transmission is close to the critical value of 1. Simulation results for 20–60% vaccination with live influenza vaccine of 2–17 year old children in Germany, averaged over 10 years (2017–26), confirm this result: four to seven times as many influenza cases are prevented among non-vaccinated individuals as among vaccinees. For complications like death due to influenza which occur much more frequently in the unvaccinated elderly than in the vaccination target group of children, indirect benefits can surpass direct ones by a factor of 20 or even more than 30.

Conclusions

The true effect of vaccination can be much bigger than what would be expected by only looking at vaccination coverage and vaccine efficacy.
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Literature
1.
go back to reference Piedra PA, Gaglani MJ, Kozinetz CA, Herschler G, Riggs M, Griffith M, Fewlass C, Watts M, Hessel C, Cordova J, et al. Herd immunity in adults against influenza-related illnesses with use of the trivalent-live attenuated influenza vaccine (CAIV-T) in children. Vaccine. 2005;23(13):1540–8.CrossRefPubMed Piedra PA, Gaglani MJ, Kozinetz CA, Herschler G, Riggs M, Griffith M, Fewlass C, Watts M, Hessel C, Cordova J, et al. Herd immunity in adults against influenza-related illnesses with use of the trivalent-live attenuated influenza vaccine (CAIV-T) in children. Vaccine. 2005;23(13):1540–8.CrossRefPubMed
2.
go back to reference Loeb M, Russell ML, Moss L, Fonseca K, Fox J, Earn DJ, Aoki F, Horsman G, Van Caeseele P, Chokani K, et al. Effect of influenza vaccination of children on infection rates in Hutterite communities: a randomized trial. JAMA. 2010;303(10):943–50.CrossRefPubMed Loeb M, Russell ML, Moss L, Fonseca K, Fox J, Earn DJ, Aoki F, Horsman G, Van Caeseele P, Chokani K, et al. Effect of influenza vaccination of children on infection rates in Hutterite communities: a randomized trial. JAMA. 2010;303(10):943–50.CrossRefPubMed
3.
go back to reference Reichert TA, Sugaya N, Fedson DS, Glezen WP, Simonsen L, Tashiro M. The Japanese experience with vaccinating schoolchildren against influenza. N Engl J Med. 2001;344(12):889–96.CrossRefPubMed Reichert TA, Sugaya N, Fedson DS, Glezen WP, Simonsen L, Tashiro M. The Japanese experience with vaccinating schoolchildren against influenza. N Engl J Med. 2001;344(12):889–96.CrossRefPubMed
4.
go back to reference Pebody R, Warburton F, Andrews N, Ellis J, von Wissmann B, Robertson C, Yonova I, Cottrell S, Gallagher N, Green H, et al. Effectiveness of seasonal influenza vaccine in preventing laboratory-confirmed influenza in primary care in the United Kingdom: 2014/15 end of season results. Euro Surveill. 2015;20(36):1–11. Pebody R, Warburton F, Andrews N, Ellis J, von Wissmann B, Robertson C, Yonova I, Cottrell S, Gallagher N, Green H, et al. Effectiveness of seasonal influenza vaccine in preventing laboratory-confirmed influenza in primary care in the United Kingdom: 2014/15 end of season results. Euro Surveill. 2015;20(36):1–11.
5.
go back to reference Weycker D, Edelsberg J, Halloran ME, Longini Jr IM, Nizam A, Ciuryla V, Oster G. Population-wide benefits of routine vaccination of children against influenza. Vaccine. 2005;23(10):1284–93.CrossRefPubMed Weycker D, Edelsberg J, Halloran ME, Longini Jr IM, Nizam A, Ciuryla V, Oster G. Population-wide benefits of routine vaccination of children against influenza. Vaccine. 2005;23(10):1284–93.CrossRefPubMed
6.
go back to reference Pradas-Velasco R, Antonanzas-Villar F, Martinez-Zarate MP. Dynamic modelling of infectious diseases: an application to the economic evaluation of influenza vaccination. PharmacoEconomics. 2008;26(1):45–56.CrossRefPubMed Pradas-Velasco R, Antonanzas-Villar F, Martinez-Zarate MP. Dynamic modelling of infectious diseases: an application to the economic evaluation of influenza vaccination. PharmacoEconomics. 2008;26(1):45–56.CrossRefPubMed
7.
go back to reference Pitman RJ, White LJ, Sculpher M. Estimating the clinical impact of introducing paediatric influenza vaccination in England and Wales. Vaccine. 2012;30(6):1208–24.CrossRefPubMed Pitman RJ, White LJ, Sculpher M. Estimating the clinical impact of introducing paediatric influenza vaccination in England and Wales. Vaccine. 2012;30(6):1208–24.CrossRefPubMed
8.
go back to reference Jordan R, Connock M, Albon E, Fry-Smith A, Olowokure B, Hawker J, Burls A. Universal vaccination of children against influenza: are there indirect benefits to the community? A systematic review of the evidence. Vaccine. 2006;24(8):1047–62.CrossRefPubMed Jordan R, Connock M, Albon E, Fry-Smith A, Olowokure B, Hawker J, Burls A. Universal vaccination of children against influenza: are there indirect benefits to the community? A systematic review of the evidence. Vaccine. 2006;24(8):1047–62.CrossRefPubMed
9.
go back to reference Vynnycky E, Pitman R, Siddiqui R, Gay N, Edmunds WJ. Estimating the impact of childhood influenza vaccination programmes in England and Wales. Vaccine. 2008;26(41):5321–30.CrossRefPubMed Vynnycky E, Pitman R, Siddiqui R, Gay N, Edmunds WJ. Estimating the impact of childhood influenza vaccination programmes in England and Wales. Vaccine. 2008;26(41):5321–30.CrossRefPubMed
10.
go back to reference Pitman RJ, Nagy LD, Sculpher MJ. Cost-effectiveness of childhood influenza vaccination in England and Wales: results from a dynamic transmission model. Vaccine. 2013;31(6):927–42. Pitman RJ, Nagy LD, Sculpher MJ. Cost-effectiveness of childhood influenza vaccination in England and Wales: results from a dynamic transmission model. Vaccine. 2013;31(6):927–42.
11.
go back to reference Gerlier L, Lamotte M, Dos Santos MS, Damm O, Schwehm M, Eichner M. Estimates of the public health impact of a pediatric vaccination program using an intranasal tetravalent live-attenuated influenza vaccine in Belgium. Paediatr Drugs. 2016;18(4):303–18.CrossRefPubMed Gerlier L, Lamotte M, Dos Santos MS, Damm O, Schwehm M, Eichner M. Estimates of the public health impact of a pediatric vaccination program using an intranasal tetravalent live-attenuated influenza vaccine in Belgium. Paediatr Drugs. 2016;18(4):303–18.CrossRefPubMed
12.
go back to reference Rose MA, Damm O, Greiner W, Knuf M, Wutzler P, Liese JG, Kruger H, Wahn U, Schaberg T, Schwehm M, et al. The epidemiological impact of childhood influenza vaccination using live-attenuated influenza vaccine (LAIV) in Germany: predictions of a simulation study. BMC Infect Dis. 2014;14:40.CrossRefPubMedPubMedCentral Rose MA, Damm O, Greiner W, Knuf M, Wutzler P, Liese JG, Kruger H, Wahn U, Schaberg T, Schwehm M, et al. The epidemiological impact of childhood influenza vaccination using live-attenuated influenza vaccine (LAIV) in Germany: predictions of a simulation study. BMC Infect Dis. 2014;14:40.CrossRefPubMedPubMedCentral
13.
go back to reference Eichner M, Schwehm M, Hain J, Uphoff H, Salzberger B, Knuf M, Schmidt-Ott R. 4Flu - an individual based simulation tool to study the effects of quadrivalent vaccination on seasonal influenza in Germany. BMC Infect Dis. 2014;14:365.CrossRefPubMedPubMedCentral Eichner M, Schwehm M, Hain J, Uphoff H, Salzberger B, Knuf M, Schmidt-Ott R. 4Flu - an individual based simulation tool to study the effects of quadrivalent vaccination on seasonal influenza in Germany. BMC Infect Dis. 2014;14:365.CrossRefPubMedPubMedCentral
15.
go back to reference Damm O, Eichner M, Rose MA, Knuf M, Wutzler P, Liese JG, Kruger H, Greiner W. Public health impact and cost-effectiveness of intranasal live attenuated influenza vaccination of children in Germany. Eur J Health Econ. 2015;16(5):471–88.CrossRefPubMed Damm O, Eichner M, Rose MA, Knuf M, Wutzler P, Liese JG, Kruger H, Greiner W. Public health impact and cost-effectiveness of intranasal live attenuated influenza vaccination of children in Germany. Eur J Health Econ. 2015;16(5):471–88.CrossRefPubMed
16.
go back to reference Statistisches Bundesamt: Bevölkerung Deutschlands bis 2060. 12. koordinierte Bevölkerungsvorausberechnung. In.; 2009. Statistisches Bundesamt: Bevölkerung Deutschlands bis 2060. 12. koordinierte Bevölkerungsvorausberechnung. In.; 2009.
17.
go back to reference Mossong J, Hens N, Jit M, Beutels P, Auranen K, Mikolajczyk R, Massari M, Salmaso S, Tomba GS, Wallinga J, et al. Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med. 2008;5(3):e74.CrossRefPubMedPubMedCentral Mossong J, Hens N, Jit M, Beutels P, Auranen K, Mikolajczyk R, Massari M, Salmaso S, Tomba GS, Wallinga J, et al. Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med. 2008;5(3):e74.CrossRefPubMedPubMedCentral
18.
go back to reference Schröder-Bernhardi D, Grunow SS, Bauman U, Zöllner Y: Schutzimpfungen gegen Influenza werden bei Kindern und Jugendlichen äußerst selten durchgeführt – Ergebnisse einer Datenbankanalyse. In: 9 Jahrestagung der Deutschen Gesellschaft für Epidemiologie. Ulm; 2014. Schröder-Bernhardi D, Grunow SS, Bauman U, Zöllner Y: Schutzimpfungen gegen Influenza werden bei Kindern und Jugendlichen äußerst selten durchgeführt – Ergebnisse einer Datenbankanalyse. In: 9 Jahrestagung der Deutschen Gesellschaft für Epidemiologie. Ulm; 2014.
19.
go back to reference Bodeker B, Remschmidt C, Muters S, Wichmann O. Influenza, tetanus, and pertussis vaccination coverage among adults in Germany. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2015;58(2):174–81.CrossRefPubMed Bodeker B, Remschmidt C, Muters S, Wichmann O. Influenza, tetanus, and pertussis vaccination coverage among adults in Germany. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2015;58(2):174–81.CrossRefPubMed
20.
go back to reference Reuss AM, Walter D, Feig M, Kappelmayer L, Buchholz U, Eckmanns T, Poggensee G. Influenza vaccination coverage in the 2004/05, 2005/06, and 2006/07 seasons: a secondary data analysis based on billing data of the German associations of statutory health insurance physicians. Dtsch Arztebl Int. 2010;107(48):845–50.PubMedPubMedCentral Reuss AM, Walter D, Feig M, Kappelmayer L, Buchholz U, Eckmanns T, Poggensee G. Influenza vaccination coverage in the 2004/05, 2005/06, and 2006/07 seasons: a secondary data analysis based on billing data of the German associations of statutory health insurance physicians. Dtsch Arztebl Int. 2010;107(48):845–50.PubMedPubMedCentral
21.
go back to reference Jefferson T, Rivetti A, Harnden A, Di Pietrantonj C, Demicheli V. Vaccines for preventing influenza in healthy children. Cochrane Database Syst Rev. 2008;2:CD004879. Jefferson T, Rivetti A, Harnden A, Di Pietrantonj C, Demicheli V. Vaccines for preventing influenza in healthy children. Cochrane Database Syst Rev. 2008;2:CD004879.
22.
go back to reference Jefferson T, Di Pietrantonj C, Rivetti A, Bawazeer GA, Al-Ansary LA, Ferroni E. Vaccines for preventing influenza in healthy adults. Cochrane Database Syst Rev. 2014;7:CD001269. Jefferson T, Di Pietrantonj C, Rivetti A, Bawazeer GA, Al-Ansary LA, Ferroni E. Vaccines for preventing influenza in healthy adults. Cochrane Database Syst Rev. 2014;7:CD001269.
23.
go back to reference Jefferson T, Di Pietrantonj C, Al-Ansary LA, Ferroni E, Thorning S, Thomas RE. Vaccines for preventing influenza in the elderly. Cochrane Database Syst Rev. 2010;2:CD004876. Jefferson T, Di Pietrantonj C, Al-Ansary LA, Ferroni E, Thorning S, Thomas RE. Vaccines for preventing influenza in the elderly. Cochrane Database Syst Rev. 2010;2:CD004876.
24.
go back to reference Jefferson T, Rivetti A, Di Pietrantonj C, Demicheli V, Ferroni E. Vaccines for preventing influenza in healthy children. Cochrane Database Syst Rev. 2012;8:CD004879. Jefferson T, Rivetti A, Di Pietrantonj C, Demicheli V, Ferroni E. Vaccines for preventing influenza in healthy children. Cochrane Database Syst Rev. 2012;8:CD004879.
25.
go back to reference Rhorer J, Ambrose CS, Dickinson S, Hamilton H, Oleka NA, Malinoski FJ, Wittes J. Efficacy of live attenuated influenza vaccine in children: a meta-analysis of nine randomized clinical trials. Vaccine. 2009;27(7):1101–10.CrossRefPubMed Rhorer J, Ambrose CS, Dickinson S, Hamilton H, Oleka NA, Malinoski FJ, Wittes J. Efficacy of live attenuated influenza vaccine in children: a meta-analysis of nine randomized clinical trials. Vaccine. 2009;27(7):1101–10.CrossRefPubMed
26.
go back to reference Carrat F, Vergu E, Ferguson NM, Lemaitre M, Cauchemez S, Leach S, Valleron AJ. Time lines of infection and disease in human influenza: a review of volunteer challenge studies. Am J Epidemiol. 2008;167(7):775–85.CrossRefPubMed Carrat F, Vergu E, Ferguson NM, Lemaitre M, Cauchemez S, Leach S, Valleron AJ. Time lines of infection and disease in human influenza: a review of volunteer challenge studies. Am J Epidemiol. 2008;167(7):775–85.CrossRefPubMed
27.
go back to reference Mossong J, Muller CP. Estimation of the basic reproduction number of measles during an outbreak in a partially vaccinated population. Epidemiol Infect. 2000;124(2):273–8.CrossRefPubMedPubMedCentral Mossong J, Muller CP. Estimation of the basic reproduction number of measles during an outbreak in a partially vaccinated population. Epidemiol Infect. 2000;124(2):273–8.CrossRefPubMedPubMedCentral
28.
29.
go back to reference Chowell G, Miller MA, Viboud C. Seasonal influenza in the United States, France, and Australia: transmission and prospects for control. Epidemiol Infect. 2008;136(6):852–64.CrossRefPubMed Chowell G, Miller MA, Viboud C. Seasonal influenza in the United States, France, and Australia: transmission and prospects for control. Epidemiol Infect. 2008;136(6):852–64.CrossRefPubMed
30.
go back to reference Williams CJ, Schweiger B, Diner G, Gerlach F, Haaman F, Krause G, Nienhaus A, Buchholz U: Seasonal influenza risk in hospital healthcare workers is more strongly associated with household than occupational exposures: results from a prospective cohort study in Berlin, Germany, 2006/07. BMC Infect Dis. 2010;10:8. Williams CJ, Schweiger B, Diner G, Gerlach F, Haaman F, Krause G, Nienhaus A, Buchholz U: Seasonal influenza risk in hospital healthcare workers is more strongly associated with household than occupational exposures: results from a prospective cohort study in Berlin, Germany, 2006/07. BMC Infect Dis. 2010;10:8.
31.
go back to reference Pebody RG, Green HK, Andrews N, Boddington NL, Zhao H, Yonova I, Ellis J, Steinberger S, Donati M, Elliot AJ, et al. Uptake and impact of vaccinating school age children against influenza during a season with circulation of drifted influenza a and B strains, England, 2014/15. Euro Surveill. 2015;20(39):1–11. Pebody RG, Green HK, Andrews N, Boddington NL, Zhao H, Yonova I, Ellis J, Steinberger S, Donati M, Elliot AJ, et al. Uptake and impact of vaccinating school age children against influenza during a season with circulation of drifted influenza a and B strains, England, 2014/15. Euro Surveill. 2015;20(39):1–11.
32.
go back to reference Blank PR, Schwenkglenks M, Szucs TD. Disparities in influenza vaccination coverage rates by target group in five European countries: trends over seven consecutive seasons. Infection. 2009;37(5):390–400.CrossRefPubMed Blank PR, Schwenkglenks M, Szucs TD. Disparities in influenza vaccination coverage rates by target group in five European countries: trends over seven consecutive seasons. Infection. 2009;37(5):390–400.CrossRefPubMed
33.
go back to reference Meier CR, Napalkov PN, Wegmuller Y, Jefferson T, Jick H. Population-based study on incidence, risk factors, clinical complications and drug utilisation associated with influenza in the United Kingdom. Eur J Clin Microbiol Infect Dis. 2000;19(11):834–42.CrossRefPubMed Meier CR, Napalkov PN, Wegmuller Y, Jefferson T, Jick H. Population-based study on incidence, risk factors, clinical complications and drug utilisation associated with influenza in the United Kingdom. Eur J Clin Microbiol Infect Dis. 2000;19(11):834–42.CrossRefPubMed
34.
go back to reference Sessa A, Costa B, Bamfi F, Bettoncelli G, D'Ambrosio G. The incidence, natural history and associated outcomes of influenza-like illness and clinical influenza in Italy. Fam Pract. 2001;18(6):629–34.CrossRefPubMed Sessa A, Costa B, Bamfi F, Bettoncelli G, D'Ambrosio G. The incidence, natural history and associated outcomes of influenza-like illness and clinical influenza in Italy. Fam Pract. 2001;18(6):629–34.CrossRefPubMed
35.
go back to reference Heikkinen T, Silvennoinen H, Peltola V, Ziegler T, Vainionpaa R, Vuorinen T, Kainulainen L, Puhakka T, Jartti T, Toikka P, et al. Burden of influenza in children in the community. J Infect Dis. 2004;190(8):1369–73.CrossRefPubMed Heikkinen T, Silvennoinen H, Peltola V, Ziegler T, Vainionpaa R, Vuorinen T, Kainulainen L, Puhakka T, Jartti T, Toikka P, et al. Burden of influenza in children in the community. J Infect Dis. 2004;190(8):1369–73.CrossRefPubMed
36.
go back to reference von Baum H, Schweiger B, Welte T, Marre R, Suttorp N, Pletz MW, Ewig S. How deadly is seasonal influenza-associated pneumonia? The German competence network for community-acquired pneumonia. Eur Respir J. 2011;37(5):1151–7.CrossRef von Baum H, Schweiger B, Welte T, Marre R, Suttorp N, Pletz MW, Ewig S. How deadly is seasonal influenza-associated pneumonia? The German competence network for community-acquired pneumonia. Eur Respir J. 2011;37(5):1151–7.CrossRef
37.
go back to reference Ewig S, Birkner N, Strauss R, Schaefer E, Pauletzki J, Bischoff H, Schraeder P, Welte T, Hoeffken G. New perspectives on community-acquired pneumonia in 388 406 patients. Results from a nationwide mandatory performance measurement programme in healthcare quality. Thorax. 2009;64(12):1062–9.CrossRefPubMedPubMedCentral Ewig S, Birkner N, Strauss R, Schaefer E, Pauletzki J, Bischoff H, Schraeder P, Welte T, Hoeffken G. New perspectives on community-acquired pneumonia in 388 406 patients. Results from a nationwide mandatory performance measurement programme in healthcare quality. Thorax. 2009;64(12):1062–9.CrossRefPubMedPubMedCentral
Metadata
Title
Direct and indirect effects of influenza vaccination
Authors
Martin Eichner
Markus Schwehm
Linda Eichner
Laetitia Gerlier
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2399-4

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