Spatiotemporal trends and climatic factors of hemorrhagic fever with renal syndrome epidemic in Shandong Province, China

Abstract

Background: Hemorrhagic fever with renal syndrome (HFRS) is a rodent-borne disease caused by Hantaviruses. It is endemic in all 31 provinces, autonomous regions, and metropolitan areas in mainland China where human cases account for 90% of the total global cases. Shandong Province is among the most serious endemic areas. HFRS cases in Shandong Province were first reported in Yutai County in 1968. Since then, the disease has spread across the province, and as of 2005, all 111 counties were reported to have local human infections. However, causes underlying such rapid spread and wide distribution remain less well understood.

Methods and findings: Here we report a spatiotemporal analysis of human HFRS cases in Shandong using data spanning 1973 to 2005. Seasonal incidence maps and velocity vector maps were produced to analyze the spread of HFRS over time in Shandong Province, and a panel data analysis was conducted to explore the association between HFRS incidence and climatic factors. Results show a rapid spread of HFRS from its epicenter in Rizhao, Linyi, Weifang Regions in southern Shandong to north, east, and west parts of the province. Based on seasonal shifts of epidemics, three epidemic phases were identified over the 33-year period. The first phase occurred between 1973 and 1982 during which the foci of HFRS was located in the south Shandong and the epidemic peak occurred in the fall and winter, presenting a seasonal characteristic of Hantaan virus (HTNV) transmission. The second phase between 1983 and 1985 was characterized by northward and westward spread of HFRS foci, and increases in incidence of HFRS in both fall-winter and spring seasons. The human infections in the spring reflected a characteristic pattern of Seoul virus (SEOV) transmission. The third phase between 1986 and 2005 was characterized by the northeast spread of the HFRS foci until it covered all counties, and the HFRS incidence in the fall-winter season decreased while it remained high in the spring. In addition, our findings suggest that precipitation, humidity, and temperature are major environmental variables that are associated with the seasonal variation of HFRS incidence in Shandong Province.

Conclusions: The spread of HFRS in Shandong Province may have been accompanied by seasonal shifts of HTNV-dominated transmission to SEOV-dominated transmission over the past three decades. The variations in HFRS incidence were significantly associated with local precipitation, humidity, and temperature.

Figure 1. The location of study area, Shandong Province in mainland China.

Figure 2. Temporal distribution patterns of HFRS incidence in Shandong Province.

(a) The figure shows the monthly epidemic curve and two notable seasonal shifts of HFRS incidence from 1973 to 2005. The time of the beginning of the economic transformation and of farm mechanization was marked by green dashed and purple dashed lines, respectively. Economic transformation mainly referred to the establishment of the household responsibility contract system (e.g. holding a household fully responsible for farmland they work); the system dramatically increased farm yields and contributed enormously to the rural economy. Farm mechanization refers to the adoption of mechanized agriculture, which largely changed agricultural patterns and human behaviors. (b) The seasonal epidemic patterns for the three phases. Average monthly epidemic curves indicate the seasonal patterns of HFRS incidence and shifts of epidemic peaks of HFRS in the three phases.

Figure 3. The spatial distribution of HFRS incidence and their proportion of monthly incidence in each county for three phases.

The background of maps with color gradient presents the annual incidence of HFRS for each phase, and pie graphs display the proportion of monthly incidences for each county. Counties in white on the map have zero incidence. * Average annual incidence per 100,000 populations. † Proportion of average monthly incidence in these pie graphs, where green color indicates the proportion of average monthly incidence from February to June (in spring and early summer), light blue is the proportion of average monthly incidence from July to August (in summer), and the red represents the proportion of average monthly incidence from September to January (in autumn and winter).

Figure 4. Spatial trends of HFRS expansion in endemic areas of Shandong Province from 1968 to 2005.

(a) The spatial dynamics of endemic areas of HFRS per decade presented by color gradients from 1968 to 2005 in Shandong Province, the numbers represent orders ranked by the month of first case reported in these counties. (b) The vector diagram of the spatial spread of endemic areas. Arrows and their lengths present the expansion direction of HFRS endemic areas and the average annual speed of diffusion of each location since the year where HFRS cases were reported, respectively.