Vaccination and the dynamics of immune evasion

Vaccines exert strong selective pressures on pathogens, favouring the spread of antigenic variants. We propose a simple mathematical model to investigate the dynamics of a novel pathogenic strain that emerges in a population where a previous strain is maintained at low endemic level by a vaccine. We compare three methods to assess the ability of the novel strain to invade and persist: algebraic rate of invasion; deterministic dynamics; and stochastic dynamics. These three techniques provide complementary predictions on the fate of the system. In particular, we emphasize the importance of stochastic simulations, which account for the possibility of extinctions of either strain. More specifically, our model suggests that the probability of persistence of an invasive strain (i) can be minimized for intermediate levels of vaccine cross-protection (i.e. immune protection against the novel strain) and (ii) is lower if cross-immunity acts through a reduced infectious period rather than through reduced susceptibility.

[1]  I. Brook,et al.  Frequency of recovery of pathogens causing acute maxillary sinusitis in adults before and after introduction of vaccination of children with the 7-valent pneumococcal vaccine. , 2006, Journal of medical microbiology.

[2]  Jer-Jea Yan,et al.  Molecular epidemiology of Bordetella pertussis in Taiwan, 1993-2004: suggests one possible explanation for the outbreak of pertussis in 1997. , 2006, Microbes and infection.

[3]  F. Mooi,et al.  Differences of circulating Bordetella pertussis population in Argentina from the strain used in vaccine production. , 2006, Vaccine.

[4]  J. Wylie,et al.  Invasive Haemophilus influenzae in Manitoba, Canada, in the Postvaccination Era , 2006, Journal of Clinical Microbiology.

[5]  B. Grenfell,et al.  Integrating life history and cross-immunity into the evolutionary dynamics of pathogens , 2006, Proceedings of the Royal Society B: Biological Sciences.

[6]  C. Yurdaydın,et al.  The first identified hepatitis B virus vaccine escape mutation in Turkey. , 2006, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[7]  W. Schaffner,et al.  Changes in Invasive Pneumococcal Disease among HIV-Infected Adults Living in the Era of Childhood Pneumococcal Immunization , 2006, Annals of Internal Medicine.

[8]  A. Galvani,et al.  Vaccination against multiple HPV types. , 2005, Mathematical biosciences.

[9]  J. Mertsola,et al.  Strain Variation among Bordetella pertussis Isolates in Finland, Where the Whole-Cell Pertussis Vaccine Has Been Used for 50 Years , 2005, Journal of Clinical Microbiology.

[10]  I. de Filippis,et al.  Occurrence of Haemophilus influenzae strains in three Brazilian states since the introduction of a conjugate Haemophilus influenzae type b vaccine. , 2005, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[11]  Laith J. Abu-Raddad,et al.  The impact of cross-immunity, mutation and stochastic extinction on pathogen diversity , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  K. Auranen,et al.  The influence of competition and vaccination on the coexistence of two pneumococcal serotypes , 2004, Epidemiology and Infection.

[13]  A. Lapedes,et al.  Mapping the Antigenic and Genetic Evolution of Influenza Virus , 2004, Science.

[14]  Nico Stollenwerk,et al.  Diversity in pathogenicity can cause outbreaks of meningococcal disease. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[15]  L. Allen,et al.  Coexistence of multiple pathogen strains in stochastic epidemic models with density-dependent mortality , 2004, Bulletin of mathematical biology.

[16]  N. Fry,et al.  Sequence variation and conservation in virulence-related genes of Bordetella pertussis isolates from the UK. , 2004, Journal of medical microbiology.

[17]  B. Grenfell,et al.  Loss of immunity to pertussis in a rural community in Senegal. , 2004, Vaccine.

[18]  O. Pybus,et al.  Unifying the Epidemiological and Evolutionary Dynamics of Pathogens , 2004, Science.

[19]  J. Gog,et al.  Population dynamics of rapid fixation in cytotoxic T lymphocyte escape mutants of influenza A , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Seyed M. Moghadas,et al.  A mathematical study of a model for childhood diseases with non-permanent immunity , 2003 .

[21]  G. De Serres,et al.  Strain Variation among Bordetella pertussis Isolates from Québec and Alberta Provinces of Canada from 1985 to 1994 , 2003, Journal of Clinical Microbiology.

[22]  Bryan T Grenfell,et al.  Dynamics and selection of many-strain pathogens , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Gog,et al.  The onset of oscillatory dynamics in models of multiple disease strains , 2002, Journal of mathematical biology.

[24]  Ingemar Nåsell,et al.  Stochastic models of some endemic infections. , 2002, Mathematical biosciences.

[25]  M. Keeling,et al.  The Interplay between Determinism and Stochasticity in Childhood Diseases , 2002, The American Naturalist.

[26]  Graham F Medley,et al.  On the determinants of population structure in antigenically diverse pathogens , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  O. Bjørnstad,et al.  Travelling waves and spatial hierarchies in measles epidemics , 2001, Nature.

[28]  I. V. van Loo,et al.  Temporal nucleotide changes in pertactin and pertussis toxin genes in Bordetella pertussis strains isolated from clinical cases in Poland. , 2001, Vaccine.

[29]  M. Clerici,et al.  Long-Term Pertussis-Specific Immunity after Primary Vaccination with a Combined Diphtheria, Tetanus, Tricomponent Acellular Pertussis, and Hepatitis B Vaccine in Comparison with That after Natural Infection , 2001, Infection and Immunity.

[30]  Tom Britton,et al.  Stochastic epidemics in dynamic populations: quasi-stationarity and extinction , 2000, Journal of mathematical biology.

[31]  T. Popović,et al.  Polymorphism in Bordetella pertussis pertactin and pertussis toxin virulence factors in the United States, 1935-1999. , 2000, The Journal of infectious diseases.

[32]  C. Oon,et al.  Hepatitis B Virus Surface Antigen (HBsAg) Mutants in Singapore Adults and Vaccinated Children with High Anti-Hepatitis B Virus Antibody Levels but Negative for HBsAg , 2000, Journal of Clinical Microbiology.

[33]  R. Singleton,et al.  Invasive Haemophilus influenzae disease in Alaskan residents aged 10 years and older before and after infant vaccination programs. , 2000, JAMA.

[34]  Michael A. Gibson,et al.  Efficient Exact Stochastic Simulation of Chemical Systems with Many Species and Many Channels , 2000 .

[35]  H. Hsu,et al.  Changes of hepatitis B surface antigen variants in carrier children before and after universal vaccination in taiwan , 1999, Hepatology.

[36]  D. Earn,et al.  Opposite patterns of synchrony in sympatric disease metapopulations. , 1999, Science.

[37]  R. Huebner,et al.  Immunogenicity and impact on nasopharyngeal carriage of a nonavalent pneumococcal conjugate vaccine. , 1999, The Journal of infectious diseases.

[38]  C. Howard,et al.  A hepatitis B virus variant found in the sera of immunised children induces a conformational change in the HbsAG “a” determinant , 1999, Journal of medical virology.

[39]  F. Mooi,et al.  Antigenic variants in Bordetella pertussis strains isolated from vaccinated and unvaccinated children. , 1999, Microbiology.

[40]  D. Nokes,et al.  The predicted pattern of emergence of vaccine-resistant hepatitis B: a cause for concern? , 1999, Vaccine.

[41]  N. Ferguson,et al.  The effect of antibody-dependent enhancement on the transmission dynamics and persistence of multiple-strain pathogens. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  L. White,et al.  Cross immunity and vaccination against multiple microparasite strains. , 1998, IMA journal of mathematics applied in medicine and biology.

[43]  N. Ferguson,et al.  Chaos, persistence, and evolution of strain structure in antigenically diverse infectious agents. , 1998, Science.

[44]  F. Mooi,et al.  Polymorphism in the Bordetella pertussisVirulence Factors P.69/Pertactin and Pertussis Toxin in The Netherlands: Temporal Trends and Evidence for Vaccine-Driven Evolution , 1998, Infection and Immunity.

[45]  N. Ferguson,et al.  Vaccination and the population structure of antigenically diverse pathogens that exchange genetic material , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[46]  Simon A. Levin,et al.  The dynamics of cocirculating influenza strains conferring partial cross-immunity , 1997, Journal of mathematical biology.

[47]  M. Lipsitch,et al.  Vaccination against colonizing bacteria with multiple serotypes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[48]  B. T. Grenfell,et al.  Disease Extinction and Community Size: Modeling the Persistence of Measles , 1997, Science.

[49]  S. Obaro,et al.  Carriage of pneumococci after pneumococcal vaccination , 1996, The Lancet.

[50]  A. McLean Vaccination, evolution and changes in the efficacy of vaccines: a theoretical framework , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  A. J. Hall Infectious diseases of humans: R. M. Anderson & R. M. May. Oxford etc.: Oxford University Press, 1991. viii + 757 pp. Price £50. ISBN 0-19-854599-1 , 1992 .

[52]  A. Zuckerman,et al.  Vaccine-induced escape mutant of hepatitis B virus , 1990, The Lancet.

[53]  B T Grenfell,et al.  Pertussis in England and Wales: an investigation of transmission dynamics and control by mass vaccination , 1989, Proceedings of the Royal Society of London. B. Biological Sciences.

[54]  D. Gillespie Exact Stochastic Simulation of Coupled Chemical Reactions , 1977 .

[55]  Denis Mollison,et al.  Spatial Contact Models for Ecological and Epidemic Spread , 1977 .

[56]  Maurice S. Bartlett,et al.  Stochastic Processes or the Statistics of Change , 1953 .

[57]  Harry Jerome Production , 1929, American Journal of Sociology.

[58]  C. J. McGrath,et al.  Effect of exchange rate return on volatility spill-over across trading regions , 2012 .

[59]  O. A. van Herwaarden,et al.  Stochastic epidemics: the probability of extinction of an infectious disease at the end of a major outbreak , 1997, Journal of mathematical biology.