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Pertussis immunity and epidemiology: mode and duration of vaccine-induced immunity

Published online by Cambridge University Press:  04 September 2015

F. M. G. MAGPANTAY ,
M. DOMENECH DE CELLÈS ,
P. ROHANI  and
A. A. KING
F. M. G. MAGPANTAY
Affiliation:
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA
M. DOMENECH DE CELLÈS
Affiliation:
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA
P. ROHANI
Affiliation:
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA Center for the Study of Complex Systems, University of Michigan, Ann Arbor, MI 48109, USA Fogarty International Center, National Institutes of Health, Bethesda, MD 20892, USA
A. A. KING*
Affiliation:
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA Center for the Study of Complex Systems, University of Michigan, Ann Arbor, MI 48109, USA Fogarty International Center, National Institutes of Health, Bethesda, MD 20892, USA Department of Mathematics, University of Michigan, Ann Arbor, MI 48109, USA
*
*Corresponding author. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA. E-mail: kingaa@umich.edu
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Summary

The resurgence of pertussis in some countries that maintain high vaccination coverage has drawn attention to gaps in our understanding of the epidemiological effects of pertussis vaccines. In particular, major questions surround the nature, degree and durability of vaccine protection. To address these questions, we used mechanistic transmission models to examine regional time series incidence data from Italy in the period immediately following the introduction of acellular pertussis (aP) vaccine. Our results concur with recent animal-challenge experiments wherein infections in aP-vaccinated individuals proved as transmissible as those in naive individuals but much less symptomatic. On the other hand, the data provide evidence for vaccine-driven reduction in susceptibility, which we quantify via a synthetic measure of vaccine impact. As to the precise nature of vaccine failure, the data do not allow us to distinguish between leakiness and waning of vaccine immunity, or some combination of these. Across the range of well-supported models, the nature and duration of vaccine protection, the age profile of incidence and the range of projected epidemiological futures differ substantially, underscoring the importance of the remaining unknowns. We identify key data gaps: sources of data that can supply the information needed to eliminate these remaining uncertainties.

Keywords

pertussisimperfect vaccineleaky vaccinewaning immunitydisease dynamicsiterated filteringlikelihood-based inference
Type
Special Issue Article
Information
Parasitology , Volume 143 , Special Issue 7: Mathematical modelling of infectious diseases , June 2016 , pp. 835 - 849
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Althouse, B. M. and Scarpino, S. V. (2015). Epidemiological consequences of an ineffective Bordetella pertussis vaccine. BMC Medicine 13, 1–12. URL http://arxiv.org/abs/1402.7332 Google Scholar
Anderson, R. M. and May, R. M. (1991). Infectious Diseases of Humans. Oxford University Press, Oxford.Google Scholar
Blackwood, J. C., Cummings, D. A. T., Broutin, H., Iamsirithaworn, S. and Rohani, P. (2012). The population ecology of infectious diseases: pertussis in Thailand as a case study. Parasitology 139, 1888–1898.Google Scholar
Blackwood, J. C., Cummings, D. A. T., Broutin, H., Iamsirithaworn, S. and Rohani, P. (2013). Deciphering the impacts of vaccination and immunity on pertussis epidemiology in Thailand. Proceedings of the National Academy of Sciences 110, 9595–9600.CrossRefGoogle ScholarPubMed
Broutin, H., Guegan, J.-F., Elguero, E., Simondon, F. and Cazelles, B. (2005). Large- scale comparative analysis of pertussis population dynamics: periodicity, synchrony, and impact of vaccination. American Journal of Epidemiology 161, 1159–1167.Google Scholar
Broutin, H., Viboud, C., Grenfell, B. T., Miller, M. A. and Rohani, P. (2010). Impact of vaccination and birth rate on the epidemiology of pertussis: a comparative study in 64 countries. Proceedings of the Royal Society of London B 277, 3239–3245.Google ScholarPubMed
Carlsson, R.-M. and Trollfors, B. (2009). Control of pertussis: lessons learnt from a 10-year surveillance programme in Sweden. Vaccine 27, 5709–5718.CrossRefGoogle ScholarPubMed
Celentano, L. P., Massari, M., Paramatti, D., Salmaso, S. and Tossi, A. E. (2005). Resurgence of pertussis in Europe. Pediatric Infectious Disease Journal 24, 761–765.Google Scholar
Cherry, J. D. (2012). Epidemic pertussis in 2012–the resurgence of a vaccine-preventable disease. The New England Journal of Medicine 367, 785–787.Google Scholar
Domenech de Cellès, M., Riolo, M., Magpantay, F. M. G., Rohani, P. and King, A. (2014). Epidemiological evidence for herd immunity induced by acellular pertussis vaccines. Proceedings of the National Academy of Sciences of the United States of America 111, E716–E717.Google Scholar
Edwards, K. M. and Decker, M. D. (2013). Vaccines, 6th Edn. chap. 21, pp. 467–475. Elsevier, available online at: http://www.sciencedirect.com/science/book/9781455700905 Google ScholarPubMed
European Commission (2014). Regional Statistics. URL http://ec.europa.eu/eurostat/data/database Google Scholar
Farrington, C. P. (2003). On vaccine efficacy and reproduction numbers. Mathematical Biosciences 185, 89–109.CrossRefGoogle ScholarPubMed
Gabutti, G. and Rota, M. C. (2012). Pertussis: a review of disease epidemiology worldwide and in Italy. International Journal of Environmental. Research and. Public Health 9, 4626–4638.Google Scholar
Gambhir, M., Clark, T. A., Cauchemez, S., Tartof, S. Y., Swerdlow, D. L. and Ferguson, N. M. (2015). A change in vaccine efficacy and duration of protection explains recent rises in pertussis incidence in the united states. PLoS Computational Biology 11, e1004138. URL http://dx.doi.org/10.1371%2Fjournal.pcbi.1004138 Google Scholar
Gomes, M. G. M., White, L. J. and Medley, G. F. (2004). Infection, reinfection, and vaccination under suboptimal immune protection: epidemiological perspectives. Journal of Theoretical Biology 228, 539–549.Google Scholar
Gonfiantini, M. V., Carloni, E., Gesualdo, F., Agricola, E., Rizzuto, E., Iannazzo, S., Ciofi Degli Atti, M. L., Villani, A. and Tozzi, A. E. (2014). Epidemiology of pertussis in Italy: disease trends over the last century. Euro Surveillance 19, 1–8.Google ScholarPubMed
Halloran, M. E., Haber, M. and Longini, I. M. (1992). Interpretation and estimation of vaccine efficacy under heterogeneity. American Journal of Epidemiology 136, 328–343.Google Scholar
Heffernan, J. M. and Keeling, M. J. (2009). Implications of vaccination and waning immunity. Proceedings of the Royal Society of London B 276, 2071–2080.Google Scholar
Ionides, E. L., Nguyen, D., Atchadé, Y., Stoev, S. and King, A. A. (2015). Inference for dynamic and latent variable models via iterated, perturbed Bayes maps. Proceedings of the National Academy of Sciences 112, 719–724. URL http://www.pnas.org/content/112/3/719. abstract.CrossRefGoogle ScholarPubMed
Jackson, D. W. and Rohani, P. (2013). Perplexities of pertussis: recent global epidemiological trends and their potential causes. Epidemiology and Infection 142, 672–684.Google Scholar
Keeling, M. J. and Rohani, P. (2008). Modeling Infectious Diseases: In Humans and Animals. Princeton University Press, Princeton.Google Scholar
King, A. A., Domenech de Cellès, M., Magpantay, F. M. G. and Rohani, P. (2015 a). Avoidable errors in the modelling of outbreaks of emerging pathogens, with special reference to Ebola. Proceedings of the Royal Society of London. Series B 282, 20150347.Google ScholarPubMed
King, A. A., Ionides, E. L., Bretó, C. M., Ellner, S. P., Ferrari, M. J., Kendall, E., Lavine, M., Nguyen, D., Reuman, D. C., Wearing, H. and Wood, S. N. (2015 b). pomp: Statistical Inference for Partially Observed Markov Processes. URL http://pomp.r-forge.r-project.org. R package, version 0.69–1.Google Scholar
King, A. A., Nguyen, D. and Ionides, E. L. (in press). Statistical inference for partially observed Markov processes via the R package pomp. Journal of Statistical Software URL http://pomp.r-forge.r-project.org/vignettes/pompjss.pdf Google Scholar
Lavine, J. S. and Rohani, P. (2012). Resolving pertussis immunity and vaccine effectiveness using incidence time series. Expert Review of Vaccines 11, 1319–1329.Google Scholar
Lavine, J. S., King, A. A., Andreasen, V. and Bjørnstad, O. N. (2013). Immune boosting explains regime-shifts in prevaccine-era pertussis dynamics. PLoS ONE 8, 1–8.Google Scholar
Lloyd, A. L. (2001). Realistic distributions of infectious periods in epidemic models: changing patterns of persistence and dynamics. Theoretical Population Biology 60, 59–71.Google Scholar
Magpantay, F. M. G., Riolo, M. A., Domenech de Cellès, M., King, A. A. and Rohani, P. (2014). Epidemiological consequences of imperfect vaccines for immunizing infections. SIAM Journal on Applied Mathematics 74, 1810–1830.Google Scholar
Magpantay, F. M. G. and Rohani, P. (2015). Dynamics of pertussis transmission in the United States. American Journal of Epidemiology 181, 921–931.Google Scholar
McGirr, A. A., Tuite, A. R. and Fisman, D. N. (2013). Estimation of the underlying burden of pertussis in adolescents and adults in Southern Ontario, Canada. PLoS ONE 8, e83850.Google Scholar
McLean, A. and Blower, S. M. (1993). Imperfect vaccines and herd immunity to HIV. Proceedings of the Royal Society of London B 253, 9–13.Google ScholarPubMed
McLean, A. R. (1998). Vaccines and their impact on the control of disease. British Medical Bulletin 54, 545–556.Google Scholar
Ministero della Salute (2014 a). Bollettino epidemiologico. URL http://www.salute.gov.it/malattieInfettive/bollettinoMalattie.jsp Google Scholar
Ministero della Salute (2014 b). Coperture vaccinali. URL http://www.salute.gov.it/portale/temi/p2_6.jsp?id=811&area=Malattie%20infettive&menu=vaccinazioni Google Scholar
Mooi, F. R., van der Maas, N. A. T. and de Melker, H. E. (2013). Pertussis resurgence: waning immunity and pathogen adaptation - two sides of the same coin. Epidemiology and Infection 142, 685–694.CrossRefGoogle ScholarPubMed
Mossong, J. and Muller, C. P. (2003). Modelling measles re-emergence as a result of waning of immunity in vaccinated populations. Vaccine 21, 4597–4603.CrossRefGoogle ScholarPubMed
Pittet, L. F., Emonet, S., Schrenzel, J., Siegrist, C.-A. and Posfay-Barbe, K. M. (2014). Bordetella holmesii: an under-recognised Bordetella species. Lancet Infectious Diseases 14, 510–519.Google Scholar
Plotkin, S. A. (2010). Correlates of protection induced by vaccination. Clinical and Vaccine Immunology 17, 1055–1065.CrossRefGoogle ScholarPubMed
Riolo, M. A., King, A. A. and Rohani, P. (2013). Can vaccine legacy explain the British pertussis resurgence? Vaccine 31, 5903–5908.CrossRefGoogle ScholarPubMed
Riolo, M. A. and Rohani, P. (2015). Combating pertussis resurgence: one booster vaccination schedule does not fit all. Proceedings of the National Academy of Sciences 112, E472–E477.Google Scholar
Rohani, P. and Drake, J. M. (2011). The decline and resurgence of pertussis in the US. Epidemics 3, 183–188.Google Scholar
Rohani, P., Zhong, X. and King, A. A. (2010). Contact network structure explains the changing epidemiology of pertussis. Science 330, 982–985.Google Scholar
Rota, M. C., D'Ancona, F., Massari, M., Mandolini, D., Giammancoc, A., Carbonari, P., Salmaso, S. and Ciofi degli Atti, M. L. (2005). How increased pertussis vaccination coverage is changing the epidemiology of pertussis in Italy. Vaccine 23, 5299–5305.Google Scholar
Ryan, M., Murphy, G., Ryan, E., Nilsson, L., Shackley, F., Gothefors, L., Oymar, K., Miller, E., Storsaeter, J. and Mills, K. H. (1998). Distinct t-cell subtypes induced with whole cell and acellular pertussis vaccines in children. Immunology 93, 1–10.CrossRefGoogle ScholarPubMed
Schellekens, J., von König, C. H. W. and Gardner, P. (2005). Pertussis sources of infection and routes of transmission in the vaccination era. The Pediatric Infectious Disease Journal 24, S19–S24.Google Scholar
Shapiro, E. D. (2012). Acellular vaccines and resurgence of pertussis. Journal of the American Medical Association 308, 2149–2150.Google Scholar
Smallridge, W., Rolin, O., Jacobs, N. and Harvill, E. (2014). Different effects of whole- cell and acellular vaccines on Bordetella transmission. Journal of Infectious Diseases 209, 1981–1988.Google Scholar
Warfel, J. M., Zimmerman, L. I. and Merkel, T. J. (2013). Acellular pertussis vaccines protect against disease but fail to prevent infection and transmission in a nonhuman primate model. Proceedings of the National Academy of Sciences 111, 787–792.Google Scholar
Wearing, H. and Rohani, P. (2009). Estimating the duration of pertussis immunity using epi- demiological signatures. PLoS Pathogens 5, e1000647.Google Scholar
Wearing, H. J., Rohani, P. and Keeling, M. J. (2005). Appropriate models for the management of infectious diseases. PLoS Medicine 2, 621–627.Google Scholar
Yih, W. K., Lett, S. M., des Vignes, F. N., Garrison, K. M., Sipe, P. L. and Marchant, D. (2000). The increasing incidence of pertussis in Massachusetts adolescents and adults, 1989–1998. Journal of Infectious Diseases 182, 1409–1416.CrossRefGoogle ScholarPubMed
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