Utility of R0 as a predictor of disease invasion in structured populations

Early theoretical work on disease invasion typically assumed large and well-mixed host populations. Many human and wildlife systems, however, have small groups with limited movement among groups. In these situations, the basic reproductive number, R0, is likely to be a poor predictor of a disease pandemic because it typically does not account for group structure and movement of individuals among groups. We extend recent work by combining the movement of hosts, transmission within groups, recovery from infection and the recruitment of new susceptibles into a stochastic model of disease in a host metapopulation. We focus on how recruitment of susceptibles affects disease invasion and how population structure can affect the frequency of superspreading events (SSEs). We show that the frequency of SSEs may decrease with the reduced movement and the group sizes due to the limited number of susceptible individuals available. Classification tree analysis of the model results illustrates the hierarchical nature of disease invasion in host metapopulations. First, the pathogen must effectively transmit within a group (R0>1), and then the pathogen must persist within a group long enough to allow for movement among the groups. Therefore, the factors affecting disease persistence—such as infectious period, group size and recruitment of new susceptibles—are as important as the local transmission rates in predicting the spread of pathogens across a metapopulation.

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

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

[3]  Wayne M. Getz,et al.  Epidemic Models: Thresholds and Population Regulation , 1983, The American Naturalist.

[4]  C B Begg,et al.  Statistical methods in medical diagnosis. , 1986, Critical reviews in medical informatics.

[5]  O. Diekmann,et al.  On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations , 1990, Journal of mathematical biology.

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

[7]  P. Kaye Infectious diseases of humans: Dynamics and control , 1993 .

[8]  K Dietz,et al.  The effect of household distribution on transmission and control of highly infectious diseases. , 1995, Mathematical biosciences.

[9]  G. Hess Disease in Metapopulation Models: Implications for Conservation , 1996 .

[10]  G. Hess Linking Extinction to Connectivity and Habitat Destruction in Metapopulation Models , 1996, The American Naturalist.

[11]  N. Becker,et al.  Optimal vaccination strategies for a community of households. , 1997, Mathematical biosciences.

[12]  H. Andersson,et al.  Epidemics in a population with social structures. , 1997, Mathematical biosciences.

[13]  F. Ball,et al.  Epidemics with two levels of mixing , 1997 .

[14]  Tom Britton,et al.  Heterogeneity in epidemic models and its effect on the spread of infection , 1998, Journal of Applied Probability.

[15]  J. Swinton Extinction times and phase transitions for spatially structured closed epidemics , 1998, Bulletin of mathematical biology.

[16]  M. Keeling,et al.  The effects of local spatial structure on epidemiological invasions , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  L Phillips,et al.  Health consequences of religious and philosophical exemptions from immunization laws: individual and societal risk of measles. , 1999, JAMA.

[18]  O. Diekmann,et al.  Mathematical Epidemiology of Infectious Diseases: Model Building, Analysis and Interpretation , 2000 .

[19]  C A Gilligan,et al.  Bubonic plague: a metapopulation model of a zoonosis , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  R. Hamman,et al.  Individual and community risks of measles and pertussis associated with personal exemptions to immunization. , 2000, JAMA.

[21]  M. Keeling,et al.  Metapopulation dynamics of bubonic plague , 2000, Nature.

[22]  J. Monahan,et al.  A Classification Tree Approach to the Development of Actuarial Violence Risk Assessment Tools , 2000, Law and human behavior.

[23]  B T Grenfell,et al.  Individual-based perspectives on R(0). , 2000, Journal of theoretical biology.

[24]  G. De’ath,et al.  CLASSIFICATION AND REGRESSION TREES: A POWERFUL YET SIMPLE TECHNIQUE FOR ECOLOGICAL DATA ANALYSIS , 2000 .

[25]  A. Dobson,et al.  Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  A. Dobson,et al.  Emerging infectious pathogens of wildlife. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  C. Gilligan,et al.  Invasion and persistence of plant parasites in a spatially structured host population , 2001 .

[28]  M E Woolhouse,et al.  Population Biology of Multihost Pathogens , 2001, Science.

[29]  S. Cornell,et al.  Dynamics of the 2001 UK Foot and Mouth Epidemic: Stochastic Dispersal in a Heterogeneous Landscape , 2001, Science.

[30]  H. McCallum,et al.  How should pathogen transmission be modelled? , 2001, Trends in ecology & evolution.

[31]  M. Keeling,et al.  Estimating spatial coupling in epidemiological systems: a mechanistic approach , 2002 .

[32]  Christopher A. Gilligan,et al.  Extinction times for closed epidemics: the effects of host spatial structure , 2002 .

[33]  O. Bjørnstad,et al.  DYNAMICS OF MEASLES EPIDEMICS: SCALING NOISE, DETERMINISM, AND PREDICTABILITY WITH THE TSIR MODEL , 2002 .

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

[35]  J A P Heesterbeek,et al.  The metapopulation dynamics of an infectious disease: tuberculosis in possums. , 2002, Theoretical population biology.

[36]  R. Schinazi,et al.  On the role of social clusters in the transmission of infectious diseases. , 2002, Theoretical population biology.

[37]  J.A.P. Heesterbeek A Brief History of R0 and a Recipe for its Calculation , 2002, Acta biotheoretica.

[38]  Mary Poss,et al.  Social Organization and Parasite Risk in Mammals: Integrating Theory and Empirical Studies , 2003 .

[39]  Wayne M. Getz,et al.  Integrating association data and disease dynamics in a social ungulate: Bovine tuberculosis in African buffalo in the Kruger National Park , 2004 .

[40]  D. Hik,et al.  Comparison of discriminant function and classification tree analyses for age classification of marmots , 2004 .

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

[42]  L Matthews,et al.  Epidemiological implications of the contact network structure for cattle farms and the 20–80 rule , 2005, Biology Letters.

[43]  M. S. Sánchez,et al.  Should we expect population thresholds for wildlife disease? , 2005, Trends in ecology & evolution.

[44]  L. Wahl,et al.  Perspectives on the basic reproductive ratio , 2005, Journal of The Royal Society Interface.

[45]  D. Watts,et al.  Multiscale, resurgent epidemics in a hierarchical metapopulation model. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. E. Kopp,et al.  Superspreading and the effect of individual variation on disease emergence , 2005, Nature.

[47]  Neo D. Martinez,et al.  Scaling up keystone effects from simple to complex ecological networks , 2005 .

[48]  N. Takamura,et al.  Predicting the distribution of invasive crayfish (Pacifastacus leniusculus) in a Kusiro Moor marsh (Japan) using classification and regression trees , 2006, Ecological Research.

[49]  L. Danon,et al.  Demographic structure and pathogen dynamics on the network of livestock movements in Great Britain , 2006, Proceedings of the Royal Society B: Biological Sciences.

[50]  Wayne M. Getz,et al.  Basic methods for modeling the invasion and spread of contagious diseases , 2006, Disease Evolution: Models, Concepts, and Data Analyses.