Demographic transition and the dynamics of measles in six provinces in China: A modeling study

Abstract

Background: Industrialization and demographic transition generate nonstationary dynamics in human populations that can affect the transmission and persistence of infectious diseases. Decades of increasing vaccination and development have led to dramatic declines in the global burden of measles, but the virus remains persistent in much of the world. Here we show that a combination of demographic transition, as a result of declining birth rates, and reduced measles prevalence, due to improved vaccination, has shifted the age distribution of susceptibility to measles throughout China.

Methods and findings: We fit a novel time-varying catalytic model to three decades of age-specific measles case reporting in six provinces in China to quantify the change in the age-specific force of infection for measles virus over time. We further quantified the impact of supplemental vaccination campaigns on the reduction of susceptible individuals. The force of infection of measles has declined dramatically (90%-97% reduction in transmission rate) in three industrialized eastern provinces during the last decade, driving a concomitant increase in both the relative proportion and absolute number of adult cases, while three central and western provinces exhibited dynamics consistent with endemic persistence (24%-73% reduction in transmission rate). The reduction in susceptible individuals due to supplemental vaccination campaigns is frequently below the nominal campaign coverage, likely because campaigns necessarily vaccinate those who may already be immune. The impact of these campaigns has significantly improved over time: campaigns prior to 2005 were estimated to have achieved less than 50% reductions in the proportion susceptible in the target age classes, but campaigns from 2005 onwards reduced the susceptible proportion by 32%-87%. A limitation of this study is that it relies on case surveillance, and thus inference may be biased by age-specific variation in measles reporting.

Conclusions: The age distribution of measles cases changes in response to both demographic and vaccination processes. Combining both processes in a novel catalytic model, we illustrate that age-specific incidence patterns reveal regional differences in the progress to measles elimination and the impact of vaccination controls in China. The shift in the age distribution of measles susceptibility in response to demographic and vaccination processes emphasizes the importance of progressive control strategies and measures to evaluate program success that anticipate and react to this transition in observed incidence.

Fig 1. National measles incidence in China.

(A) Historical measles incidence (black) and birth rate (red) in China from 1950 to 2011 collected by the China Centers for Disease Control and Prevention. (B) Map of the six focal provinces. (C) Mean percent of measles cases reported in each month for the six focal provinces from 1980 to 2011.

Fig 2. Changing age distribution of population and measles cases in six focal provinces.

(A–F) Estimated percent of population in each age class for Jiangsu, Shandong, Zhejiang, Henan, Yunnan, and Gansu Provinces from national census; white indicates years for which no age-specific measles surveillance was available. (G–L) Reported measles cases (log_e[cases + 1]) per year in each age class for six focal provinces; order and white is as in (A–F).

Fig 3. Fitted age-specific force of infection for six focal provinces.

Rows indicate Jiangsu, Shandong, Zhejiang, Henan, Yunnan, and Gansu Provinces. Columns indicate model fits for each observed decade. The fitted age-specific force of infection (FOI) is scaled to have a maximum of 1 in the decade 1991–2000 (left column); the FOI in 2001–2011 (right column) in each province is scaled relative to the values in 1991–2000. Grey shading gives the 2.5th and 97.5th percentiles of the posterior distribution of the fitted spline.

Fig 4. Estimated proportion susceptible in each age class in Jiangsu Province in 2010.

Grey shading gives the 95% credible interval for the proportion (PPN) of each age class susceptible to measles as estimated from the catalytic model fit. Circles and vertical bars indicate the point estimates and 95% confidence intervals of the proportion susceptible, by age, for the province and three of its prefectures from a serological (sero) survey conducted in 2010 as reported in Liu et al. [31,32].

Fig 5. Estimated effectiveness of supplementary immunization activities in six focal provinces.

The estimated 95% credible interval for the proportion of susceptible individuals in the targeted age class effectively immunized in each supplementary immunization activity (SIA) is given by the range of the vertical bars. Circles indicate the mean of the posterior distribution for provincial-scale SIAs. Squares indicate the same for sub-provincial SIAs. Overlapping points have been shifted in the x-dimension to permit visibility.