Stochasticity in staged models of epidemics: quantifying the dynamics of whooping cough

Although many stochastic models can accurately capture the qualitative epidemic patterns of many childhood diseases, there is still considerable discussion concerning the basic mechanisms generating these patterns; much of this stems from the use of deterministic models to try to understand stochastic simulations. We argue that a systematic method of analysing models of the spread of childhood diseases is required in order to consistently separate out the effects of demographic stochasticity, external forcing and modelling choices. Such a technique is provided by formulating the models as master equations and using the van Kampen system-size expansion to provide analytical expressions for quantities of interest. We apply this method to the susceptible–exposed–infected–recovered (SEIR) model with distributed exposed and infectious periods and calculate the form that stochastic oscillations take on in terms of the model parameters. With the use of a suitable approximation, we apply the formalism to analyse a model of whooping cough which includes seasonal forcing. This allows us to more accurately interpret the results of simulations and to make a more quantitative assessment of the predictions of the model. We show that the observed dynamics are a result of a macroscopic limit cycle induced by the external forcing and resonant stochastic oscillations about this cycle.

[1]  Matt J. Keeling,et al.  Understanding the persistence of measles: reconciling theory, simulation and observation , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  D. Earn,et al.  Interepidemic Intervals in Forced and Unforced SEIR Models , 2022 .

[3]  Pejman Rohani,et al.  Appropriate Models for the Management of Infectious Diseases , 2005, PLoS medicine.

[4]  D. B. Preston Spectral Analysis and Time Series , 1983 .

[5]  I B Schwartz,et al.  Seasonality and period-doubling bifurcations in an epidemic model. , 1984, Journal of theoretical biology.

[6]  O. Bjørnstad,et al.  Dynamics of measles epidemics: Estimating scaling of transmission rates using a time series sir model , 2002 .

[7]  H. Hethcote,et al.  Integral equation models for endemic infectious diseases , 1980, Journal of mathematical biology.

[8]  Rachel Kuske,et al.  Sustained oscillations via coherence resonance in SIR. , 2007, Journal of theoretical biology.

[9]  L. Coriell Host immunity. , 1968, Journal of pediatric surgery.

[10]  A. McKane,et al.  Extinction dynamics in mainland-island metapopulations: An N-patch stochastic model , 2002, Bulletin of mathematical biology.

[11]  J. Yorke,et al.  Recurrent outbreaks of measles, chickenpox and mumps. I. Seasonal variation in contact rates. , 1973, American journal of epidemiology.

[12]  Ralf Engbert,et al.  Chance and chaos in population biology—Models of recurrent epidemics and food chain dynamics , 1994 .

[13]  D. Earn,et al.  A simple model for complex dynamical transitions in epidemics. , 2000, Science.

[14]  M. Keeling,et al.  On methods for studying stochastic disease dynamics , 2008, Journal of The Royal Society Interface.

[15]  M. Keeling,et al.  Modeling Infectious Diseases in Humans and Animals , 2007 .

[16]  A J McKane,et al.  Predator-prey cycles from resonant amplification of demographic stochasticity. , 2005, Physical review letters.

[17]  Andrew J Black,et al.  Stochastic fluctuations in the susceptible-infective-recovered model with distributed infectious periods. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[18]  Z. Grossman,et al.  Oscillatory phenomena in a model of infectious diseases. , 1980, Theoretical population biology.

[19]  N M Ferguson,et al.  Mass vaccination to control chickenpox: the influence of zoster. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[21]  Norman T. J. Bailey ON ESTIMATING THE LATENT AND INFECTIOUS PERIODS OF MEASLES , 1956 .

[22]  J. Cherry The Epidemiology of Pertussis: A Comparison of the Epidemiology of the Disease Pertussis With the Epidemiology of Bordetella pertussis Infection , 2005, Pediatrics.

[23]  P. Fine,et al.  Seasonal influences on pertussis. , 1986, International journal of epidemiology.

[24]  M. Bartlett Measles Periodicity and Community Size , 1957 .

[25]  B. Grenfell,et al.  Seasonality and the persistence and invasion of measles , 2007, Proceedings of the Royal Society B: Biological Sciences.

[26]  J V Ross,et al.  On parameter estimation in population models. , 2006, Theoretical population biology.

[27]  M. Pascual,et al.  Stochastic amplification in epidemics , 2007, Journal of The Royal Society Interface.

[28]  O. Bjørnstad,et al.  The dynamics of measles in sub-Saharan Africa , 2008, Nature.

[29]  Mercedes Pascual,et al.  Skeletons, noise and population growth: the end of an old debate? , 2004, Trends in ecology & evolution.

[30]  R. Watson,et al.  On the spread of a disease with gamma distributed latent and infectious periods , 1980 .

[31]  J. Griffiths The Theory of Stochastic Processes , 1967 .

[32]  S. Tjoa,et al.  PRACTOLOL IN THE CONTROL OF INTRAOCULAR TENSION , 1974 .

[33]  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.

[34]  W. Gurney,et al.  Modelling fluctuating populations , 1982 .

[35]  Tobias Galla,et al.  Limit cycles, complex Floquet multipliers, and intrinsic noise. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[36]  J. Ross,et al.  Stochastic models for mainland-island metapopulations in static and dynamic landscapes , 2006, Bulletin of mathematical biology.

[37]  M. M. Telo da Gama,et al.  Stochastic fluctuations in epidemics on networks , 2007, Journal of The Royal Society Interface.

[38]  R. Simpson,et al.  Infectiousness of communicable diseases in the household (measles, chickenpox, and mumps). , 1952, Lancet.

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

[40]  H. D. Miller,et al.  The Theory Of Stochastic Processes , 1977, The Mathematical Gazette.

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

[42]  I B Schwartz,et al.  Multiple stable recurrent outbreaks and predictability in seasonally forced nonlinear epidemic models , 1985, Journal of mathematical biology.

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

[44]  Ingemar Nåsell,et al.  On the time to extinction in recurrent epidemics , 1999 .

[45]  P. Fine,et al.  Measles in England and Wales--I: An analysis of factors underlying seasonal patterns. , 1982, International journal of epidemiology.

[46]  D. Sherrington Stochastic Processes in Physics and Chemistry , 1983 .

[47]  Pejman Rohani,et al.  Seasonnally forced disease dynamics explored as switching between attractors , 2001 .

[48]  R. May,et al.  Infectious Diseases of Humans: Dynamics and Control , 1991, Annals of Internal Medicine.

[49]  R. Pebody,et al.  Recent developments in pertussis , 2006, The Lancet.

[50]  P. Hosseini,et al.  Seasonality and the dynamics of infectious diseases. , 2006, Ecology letters.

[51]  M. Keeling,et al.  Integrating stochasticity and network structure into an epidemic model , 2008, Journal of The Royal Society Interface.

[52]  H. E. Soper The Interpretation of Periodicity in Disease Prevalence , 1929 .

[53]  H. B. Wilson,et al.  Chaotic stochasticity: a ubiquitous source of unpredictability in epidemics , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[54]  B T Grenfell,et al.  Noisy Clockwork: Time Series Analysis of Population Fluctuations in Animals , 2001, Science.

[55]  D. Schenzle An age-structured model of pre- and post-vaccination measles transmission. , 1984, IMA journal of mathematics applied in medicine and biology.

[56]  P. Pollett On a model for interference between searching insect parasites , 1990, The Journal of the Australian Mathematical Society. Series B. Applied Mathematics.

[57]  D. Gillespie A General Method for Numerically Simulating the Stochastic Time Evolution of Coupled Chemical Reactions , 1976 .

[58]  N M Ferguson,et al.  Spatial heterogeneity and the persistence of infectious diseases. , 2004, Journal of theoretical biology.

[59]  A. Hastings,et al.  Stochastic Dynamics and Deterministic Skeletons: Population Behavior of Dungeness Crab , 1997 .

[60]  Alun L Lloyd,et al.  Spatiotemporal dynamics of epidemics: synchrony in metapopulation models. , 2004, Mathematical biosciences.

[61]  H G Solari,et al.  Sustained oscillations in stochastic systems. , 2001, Mathematical biosciences.

[62]  H. Hethcote,et al.  An age-structured model for pertussis transmission. , 1997, Mathematical biosciences.

[63]  A L Lloyd,et al.  Destabilization of epidemic models with the inclusion of realistic distributions of infectious periods , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[64]  N. Grassly,et al.  Host immunity and synchronized epidemics of syphilis across the United States , 2005, Nature.

[65]  P. Rohani,et al.  Noise, nonlinearity and seasonality: the epidemics of whooping cough revisited , 2008, Journal of The Royal Society Interface.

[66]  D. Earn,et al.  Transients and attractors in epidemics , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  David F Anderson,et al.  A modified next reaction method for simulating chemical systems with time dependent propensities and delays. , 2007, The Journal of chemical physics.