Rubella metapopulation dynamics and importance of spatial coupling to the risk of congenital rubella syndrome in Peru

Rubella is generally a mild childhood disease, but infection during early pregnancy may cause spontaneous abortion or congenital rubella syndrome (CRS), which may entail a variety of birth defects. Consequently, understanding the age-structured dynamics of this infection has considerable public health value. Vaccination short of the threshold for local elimination of transmission will increase the average age of infection. Accordingly, the classic concern for this infection is the potential for vaccination to increase incidence in individuals of childbearing age. A neglected aspect of rubella dynamics is how age incidence patterns may be moulded by the spatial dynamics inherent to epidemic metapopulations. Here, we use a uniquely detailed dataset from Peru to explore the implications of this for the burden of CRS. Our results show that the risk of CRS may be particularly severe in small remote regions, a prediction at odds with expectations in the endemic situation, and with implications for the outcome of vaccination. This outcome results directly from the metapopulation context: specifically, extinction–re-colonization dynamics are crucial because they allow for significant leakage of susceptible individuals into the older age classes during inter-epidemic periods with the potential to increase CRS risk by as much as fivefold.

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

[2]  Mark Bartlett,et al.  The Critical Community Size for Measles in the United States , 1960 .

[3]  W. Dowdle,et al.  WHO collaborative study on the sero-epidemiology of rubella in Caribbean and Middle and South American populations in 1968. , 1970, Bulletin of the World Health Organization.

[4]  D. Griffiths,et al.  A Catalytic Model of Infection for Measles , 1974 .

[5]  J. Best,et al.  STRATEGY FOR RUBELLA VACCINATION , 1983, The Lancet.

[6]  R M May,et al.  Vaccination against rubella and measles: quantitative investigations of different policies , 1983, Journal of Hygiene.

[7]  B T Grenfell,et al.  The estimation of age-related rates of infection from case notifications and serological data , 1985, Journal of Hygiene.

[8]  B T Grenfell,et al.  Quantitative investigations of different vaccination policies for the control of congenital rubella syndrome (CRS) in the United Kingdom , 1986, Journal of Hygiene.

[9]  M. Haine,et al.  Van Damme A. , 1986 .

[10]  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 .

[11]  B. Grenfell,et al.  (Meta)population dynamics of infectious diseases. , 1997, Trends in ecology & evolution.

[12]  T. Panagiotopoulos,et al.  Increase in congenital rubella occurrence after immunisation in Greece: retrospective survey and systematic review. , 1999, BMJ.

[13]  E. Vynnycky,et al.  Modelling the incidence of congenital rubella syndrome in developing countries. , 1999, International journal of epidemiology.

[14]  M. Kretzschmar,et al.  The pre-vaccination epidemiology of measles, mumps and rubella in Europe: implications for modelling studies , 2000, Epidemiology and Infection.

[15]  Bärbel Finkenstädt,et al.  Time series modelling of childhood diseases: a dynamical systems approach , 2000 .

[16]  S. Reef,et al.  Unseen blindness, unheard deafness, and unrecorded death and disability: congenital rubella in Kumasi, Ghana. , 2000, American journal of public health.

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

[18]  S. Plotkin Rubella eradication. , 2001, Vaccine.

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

[20]  Bryan T Grenfell,et al.  A stochastic model for extinction and recurrence of epidemics: estimation and inference for measles outbreaks. , 2002, Biostatistics.

[21]  K Glass,et al.  Interpreting time-series analyses for continuous-time biological models--measles as a case study. , 2003, Journal of theoretical biology.

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

[23]  E. Vynnycky,et al.  The predicted impact of private sector MMR vaccination on the burden of Congenital Rubella Syndrome. , 2003, Vaccine.

[24]  Y. Xia,et al.  Measles Metapopulation Dynamics: A Gravity Model for Epidemiological Coupling and Dynamics , 2004, The American Naturalist.

[25]  Ingemar Nåsell,et al.  A new look at the critical community size for childhood infections. , 2005, Theoretical population biology.

[26]  G Molenberghs,et al.  Modelling age‐dependent force of infection from prevalence data using fractional polynomials , 2006, Statistics in medicine.

[27]  L. D. de Oliveira,et al.  A rubella serosurvey in postpartum women in the three regions of Peru. , 2007, Revista panamericana de salud publica = Pan American journal of public health.

[28]  Bryan T. Grenfell,et al.  Hazards, spatial transmission and timing of outbreaks in epidemic metapopulations , 2008, Environmental and Ecological Statistics.

[29]  C. Jessica E. Metcalf,et al.  Seasonality and comparative dynamics of six childhood infections in pre-vaccination Copenhagen , 2009, Proceedings of the Royal Society B: Biological Sciences.

[30]  O. Bjørnstad,et al.  Episodic outbreaks bias estimates of age-specific force of infection: a corrected method using measles as an example , 2009, Epidemiology and Infection.

[31]  Cecile Viboud,et al.  Absolute Humidity and the Seasonal Onset of Influenza in the Continental US , 2009, PLoS currents.

[32]  G. Chowell,et al.  Spatial and Temporal Dynamics of Rubella in Peru, 1997–2006: Geographic Patterns, Age at Infection and Estimation of Transmissibility , 2009 .

[33]  O. Bjørnstad,et al.  The epidemiology of rubella in Mexico: seasonality, stochasticity and regional variation , 2010, Epidemiology and Infection.

[34]  Cécile Viboud,et al.  Absolute Humidity and the Seasonal Onset of Influenza in the Continental United States , 2010, PLoS biology.