Capturing the dynamics of pathogens with many strains

Pathogens that consist of multiple antigenic variants are a serious public health concern. These infections, which include dengue virus, influenza and malaria, generate substantial morbidity and mortality. However, there are considerable theoretical challenges involved in modelling such infections. As well as describing the interaction between strains that occurs as a result cross-immunity and evolution, models must balance biological realism with mathematical and computational tractability. Here we review different modelling approaches, and suggest a number of biological problems that are potential candidates for study with these methods. We provide a comprehensive outline of the benefits and disadvantages of available frameworks, and describe what biological information is preserved and lost under different modelling assumptions. We also consider the emergence of new disease strains, and discuss how models of pathogens with multiple strains could be developed further in future. This includes extending the flexibility and biological realism of current approaches, as well as interface with data.

[1]  G. Pawelec,et al.  Mechanisms of immunosenescence , 2009, Immunity & Ageing.

[2]  Julia R Gog,et al.  Influenza drift and epidemic size: the race between generating and escaping immunity. , 2004, Theoretical population biology.

[3]  Dinis Gökaydin,et al.  The reinfection threshold regulates pathogen diversity: the case of influenza , 2007, Journal of The Royal Society Interface.

[4]  A. Doucet,et al.  Particle Markov chain Monte Carlo methods , 2010 .

[5]  S. Halstead,et al.  Failure of secondary infection with American genotype dengue 2 to cause dengue haemorrhagic fever , 1999, The Lancet.

[6]  A. Conlan,et al.  Measuring social networks in British primary schools through scientific engagement , 2010, Proceedings of the Royal Society B: Biological Sciences.

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

[8]  Marcel Tanner,et al.  Prevalence and implications of multiple-strain infections. , 2011, The Lancet. Infectious diseases.

[9]  A. Rothman Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms , 2011, Nature Reviews Immunology.

[10]  R. May,et al.  The maintenance of strain structure in populations of recombining infectious agents , 1996, Nature Medicine.

[11]  C. Wilke,et al.  Phenotypic differences in viral immune escape explained by linking within-host dynamics to host-population immunity. , 2010, Journal of theoretical biology.

[12]  L. Elveback,et al.  AN EXTENSION OF THE REED-FROST EPIDEMIC MODEL FOR THE STUDY OF COMPETITION BETWEEN VIRAL AGENTS IN THE PRESENCE OF INTERFERENCE. , 1964, American journal of hygiene.

[13]  David L. Smith,et al.  Strain theory of malaria: the first 50 years. , 2008, Advances in parasitology.

[14]  Adam Kucharski,et al.  Influenza emergence in the face of evolutionary constraints , 2011, Proceedings of the Royal Society B: Biological Sciences.

[15]  S. Gupta,et al.  Antigenic diversity and the transmission dynamics of Plasmodium falciparum. , 1994, Science.

[16]  Francesca Tria,et al.  A minimal stochastic model for influenza evolution , 2005, q-bio/0505035.

[17]  N. Lennon,et al.  Dynamics of Dengue Disease Severity Determined by the Interplay Between Viral Genetics and Serotype-Specific Immunity , 2011, Science Translational Medicine.

[18]  W. O. Kermack,et al.  A contribution to the mathematical theory of epidemics , 1927 .

[19]  Jacob Bodilsen,et al.  [Plasmodium falciparum]. , 2022, Ugeskrift for laeger.

[20]  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.

[21]  S. Gupta,et al.  A strain theory of malaria transmission. , 1994, Parasitology today.

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

[23]  Katia Koelle,et al.  Decreases in dengue transmission may act to increase the incidence of dengue hemorrhagic fever , 2008, Proceedings of the National Academy of Sciences.

[24]  Ira B Schwartz,et al.  Dynamic effects of antibody-dependent enhancement on the fitness of viruses. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[25]  N. Andrews,et al.  Incidence of 2009 pandemic influenza A H1N1 infection in England: a cross-sectional serological study , 2010, The Lancet.

[26]  A. Sasaki,et al.  Shaping the phylogenetic tree of influenza by cross-immunity. , 2006, Theoretical population biology.

[27]  A. Kucharski,et al.  Age profile of immunity to influenza: effect of original antigenic sin. , 2012, Theoretical population biology.

[28]  Mario Recker,et al.  The Effects of Tertiary and Quaternary Infections on the Epidemiology of Dengue , 2010, PloS one.

[29]  J. Botella de Maglia,et al.  [Prevention of malaria]. , 1999, Revista clinica espanola.

[30]  Mercedes Pascual,et al.  Consequences of host heterogeneity, epitope immunodominance, and immune breadth for strain competition. , 2011, Journal of theoretical biology.

[31]  Leon Danon,et al.  Host community structure and the maintenance of pathogen diversity , 2007, Proceedings of the Royal Society B: Biological Sciences.

[32]  K Dietz,et al.  Epidemiologic interference of virus populations , 1979, Journal of mathematical biology.

[33]  Florian Krammer,et al.  Neutralizing Antibodies Against Previously Encountered Influenza Virus Strains Increase over Time: A Longitudinal Analysis , 2013, Science Translational Medicine.

[34]  Neil Ferguson,et al.  The Influence of Different Forms of Cross-Protective Immunity on the Population Dynamics of Antigenically Diverse Pathogens , 2002 .

[35]  Edward C. Holmes,et al.  Discovering the Phylodynamics of RNA Viruses , 2009, PLoS Comput. Biol..

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

[37]  C. M. Pease An evolutionary epidemiological mechanism, with applications to type A influenza. , 1987, Theoretical population biology.

[38]  Akira Sasaki,et al.  Antigenic distance and cross-immunity, invasibility and coexistence of pathogen strains in an epidemiological model with discrete antigenic space. , 2009, Theoretical population biology.

[39]  Yi Guan,et al.  Location-specific patterns of exposure to recent pre-pandemic strains of influenza A in southern China , 2011, Nature communications.

[40]  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 .

[41]  J. Banavar,et al.  Synthesizing within-host and population-level selective pressures on viral populations: the impact of adaptive immunity on viral immune escape , 2010, Journal of The Royal Society Interface.

[42]  A. Galvani,et al.  The effects of host heterogeneity on pathogen population structure. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[43]  Akira Sasaki,et al.  Why are dengue virus serotypes so distantly related? Enhancement and limiting serotype similarity between dengue virus strains , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  Neil Ferguson,et al.  Incorporating demographic stochasticity into multi-strain epidemic models: application to influenza A , 2009, Journal of The Royal Society Interface.

[45]  Mario Recker,et al.  Immunological serotype interactions and their effect on the epidemiological pattern of dengue , 2009, Proceedings of the Royal Society B: Biological Sciences.

[46]  M. Newman,et al.  Simple model of epidemics with pathogen mutation. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[47]  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.

[48]  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.

[49]  M. Feldman,et al.  Epidemic dynamics and antigenic evolution in a single season of influenza A , 2006, Proceedings of the Royal Society B: Biological Sciences.

[50]  S. Hamilton,et al.  Epidemiological models. , 1976, Indian journal of public health.

[51]  S. Levin,et al.  The SIRC model and influenza A. , 2006, Mathematical biosciences.

[52]  Katia Koelle,et al.  The effects of host contact network structure on pathogen diversity and strain structure. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Prida Malasit,et al.  Cross-Reacting Antibodies Enhance Dengue Virus Infection in Humans , 2010, Science.

[54]  Cecile Viboud,et al.  Stochastic Processes Are Key Determinants of Short-Term Evolution in Influenza A Virus , 2006, PLoS pathogens.

[55]  Viggo Andreasen,et al.  Dynamics of annual influenza A epidemics with immuno-selection , 2003, Journal of mathematical biology.

[56]  David L. Smith,et al.  Strain theory of malaria: the first 50 years. , 2008, Advances in parasitology.

[57]  I. Wilson,et al.  Structural basis of immune recognition of influenza virus hemagglutinin. , 1990, Annual review of immunology.

[58]  M. Pascual,et al.  Understanding the dynamics of rapidly evolving pathogens through modeling the tempo of antigenic change: influenza as a case study. , 2009, Epidemics.

[59]  E. Vergu,et al.  Influenza A Gradual and Epochal Evolution: Insights from Simple Models , 2009, PloS one.

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

[61]  Thomas Francis,et al.  EPIDEMIOLOGIC AND IMMUNOLOGIC SIGNIFICANCE OF AGE DISTRIBUTION OF ANTIBODY TO ANTIGENIC VARIANTS OF INFLUENZA VIRUS , 1953, The Journal of experimental medicine.

[62]  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.

[63]  Julia R. Gog,et al.  The Role of Social Contacts and Original Antigenic Sin in Shaping the Age Pattern of Immunity to Seasonal Influenza , 2012, PLoS Comput. Biol..

[64]  D. Fleming,et al.  Fatal Cases of Influenza A in Childhood , 2009, PloS one.

[65]  Thomas B. Kepler,et al.  A two-tiered model for simulating the ecological and evolutionary dynamics of rapidly evolving viruses, with an application to influenza , 2010, Journal of The Royal Society Interface.

[66]  Konstantin B. Blyuss,et al.  Stability and bifurcations in a model of antigenic variation in malaria , 2009, Journal of mathematical biology.

[67]  Elizabeth C. Theil,et al.  Epochal Evolution Shapes the Phylodynamics of Interpandemic Influenza A (H3N2) in Humans , 2006, Science.

[68]  Akira Sasaki,et al.  Cross-immunity, invasion and coexistence of pathogen strains in epidemiological models with one-dimensional antigenic space. , 2007, Mathematical biosciences.

[69]  J. Gog The impact of evolutionary constraints on influenza dynamics. , 2008, Vaccine.

[70]  J. Gog,et al.  A status-based approach to multiple strain dynamics , 2002, Journal of mathematical biology.

[71]  Konstantin B. Blyuss,et al.  The effects of symmetry on the dynamics of antigenic variation , 2012, Journal of mathematical biology.

[72]  Mario Recker,et al.  Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis , 2008, Proceedings of the National Academy of Sciences.

[73]  R. Webster,et al.  Evolution and ecology of influenza A viruses. , 1992, Current topics in microbiology and immunology.

[74]  C W Potter,et al.  Determinants of immunity to influenza infection in man. , 1979, British medical bulletin.

[75]  David A. Rasmussen,et al.  Inference for Nonlinear Epidemiological Models Using Genealogies and Time Series , 2011, PLoS Comput. Biol..

[76]  Gavin J. D. Smith,et al.  Evidence for Antigenic Seniority in Influenza A (H3N2) Antibody Responses in Southern China , 2012, PLoS pathogens.

[77]  R. Mikolajczyk,et al.  Social Contacts and Mixing Patterns Relevant to the Spread of Infectious Diseases , 2008, PLoS medicine.

[78]  Neil Ferguson,et al.  Improving the realism of deterministic multi-strain models: implications for modelling influenza A , 2008, Journal of The Royal Society Interface.

[79]  N. Cox,et al.  Antigenic drift in influenza virus H3 hemagglutinin from 1968 to 1980: multiple evolutionary pathways and sequential amino acid changes at key antigenic sites , 1983, Journal of virology.

[80]  D. Weiskopf,et al.  Biology of immune responses to vaccines in elderly persons. , 2008, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

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

[82]  Paul S. Wikramaratna,et al.  Five challenges in modelling interacting strain dynamics. , 2015, Epidemics.

[83]  Mario Recker,et al.  The generation of influenza outbreaks by a network of host immune responses against a limited set of antigenic types , 2007, Proceedings of the National Academy of Sciences.

[84]  S. Levin,et al.  Dynamics of influenza A drift: the linear three-strain model. , 1999, Mathematical biosciences.

[85]  W. O. Kermack,et al.  Contributions to the mathematical theory of epidemics—I , 1991, Bulletin of mathematical biology.

[86]  Katia Koelle,et al.  Phylodynamic Inference and Model Assessment with Approximate Bayesian Computation: Influenza as a Case Study , 2012, PLoS Comput. Biol..

[87]  James E. Crowe,et al.  Structural Basis of Preexisting Immunity to the 2009 H1N1 Pandemic Influenza Virus , 2010, Science.

[88]  Pejman Rohani,et al.  Statistical Inference for Multi-Pathogen Systems , 2011, PLoS Comput. Biol..

[89]  Trevor Bedford,et al.  Canalization of the evolutionary trajectory of the human influenza virus , 2011, BMC Biology.

[90]  Ulf Dieckmann,et al.  On State-Space Reduction in Multi-Strain Pathogen Models, with an Application to Antigenic Drift in Influenza A , 2007, PLoS Comput. Biol..

[91]  S. Levin,et al.  Epidemiological models with age structure, proportionate mixing, and cross-immunity , 1989, Journal of mathematical biology.

[92]  N. Ferguson,et al.  Ecological and immunological determinants of influenza evolution , 2003, Nature.