Geospatial characteristics of measles transmission in China during 2005−2014

Measles is a highly contagious and severe disease. Despite mass vaccination, it remains a leading cause of death in children in developing regions, killing 114,900 globally in 2014. In 2006, China committed to eliminating measles by 2012; to this end, the country enhanced its mandatory vaccination programs and achieved vaccination rates reported above 95% by 2008. However, in spite of these efforts, during the last 3 years (2013–2015) China documented 27,695, 52,656, and 42,874 confirmed measles cases. How measles manages to spread in China—the world’s largest population—in the mass vaccination era remains poorly understood. To address this conundrum and provide insights for future public health efforts, we analyze the geospatial pattern of measles transmission across China during 2005–2014. We map measles incidence and incidence rates for each of the 344 cities in mainland China, identify the key socioeconomic and demographic features associated with high disease burden, and identify transmission clusters based on the synchrony of outbreak cycles. Using hierarchical cluster analysis, we identify 21 epidemic clusters, of which 12 were cross-regional. The cross-regional clusters included more underdeveloped cities with large numbers of emigrants than would be expected by chance (p = 0.011; bootstrap sampling), indicating that cities in these clusters were likely linked by internal worker migration in response to uneven economic development. In contrast, cities in regional clusters were more likely to have high rates of minorities and high natural growth rates than would be expected by chance (p = 0.074; bootstrap sampling). Our findings suggest that multiple highly connected foci of measles transmission coexist in China and that migrant workers likely facilitate the transmission of measles across regions. This complex connection renders eradication of measles challenging in China despite its high overall vaccination coverage. Future immunization programs should therefore target these transmission foci simultaneously.Author summary: Measles is a highly infectious disease. Eradication of measles can nevertheless be achieved with vaccination of 90–95% of a population, as shown in theory and practice. In China, however, measles continues to infect thousands of people each year despite vaccination coverage above 95%. This conundrum challenges measles elimination in China and worldwide. Here we characterize the geospatial distribution of measles and epidemic connections among cities across China. Using incidence data reported during 2005–2014 for all 344 cities in China, we show that the municipal burden of measles differed substantially and some cities were highly connected and experienced synchronous outbreaks. We identify 14 cities that experienced endemic transmission during 2005–2010, and 21 transmission clusters, including 6 cross-regional clusters that link the less developed inland regions and the industrial east. We find that three transmission foci coexist in China—cities with large minority populations, inland cities with more emigrants, and mega industrial cities hosting more immigrants—and that migrant workers, connecting the latter two foci, likely facilitate measles transmission across regions. This complex connection, along with the differing disease burden among cities, renders measles elimination challenging in China despite the high overall vaccination rate. Future immunization programs should therefore target these three foci.