Background
Malaria is an important cause of death and illness in children and adults in tropical countries. According to World Malaria Report 2009[
1], half of the world's population is at risk of malaria and an estimated 243 million cases led to nearly 863,000 deaths in 2008. Despite significant reductions in the overall burden of malaria in the 20
th century, the disease still represents a significant public health problem in China [
2].
Malaria was historically epidemic in the Huang-Huai River region of central China and the total malaria cases in these areas were 21.99 million, accounting for 91.2% of the total reported cases in the country in 1970s. With active implementation of malaria control measures for more than 30 years, considerable success had been achieved and the cases decreased dramatically and many counties in Huang-Huai River region reached the standard of the basic malaria elimination (the incidence is below than 1/10,000). Early in the 21
th century, malaria has re-emerged in these areas, especially the Anhui Province, and a total 26,873 malaria cases and 108,594 suspected cases with 23 deaths were reported by the annual case reporting system in 858 counties of 22 Provinces in 2008, and the annual incidence was 0.21/10 000. In central China, the re-emergence of malaria was controlled in 2008, but the number of malaria cases and the incidence in central China still accounts for 68% of the total cases [
3]. According to a 2003 national report [
4], it was estimated that only 1/18 (5.6%) cases in China were notified and the actual number of cases was higher than reported. Besides, malaria vectors in this area included
Anopheles sinensis and
Anopheles anthropophagus historically.
In fact, social and economical status have significantly changed since 1990s in central parts of China, and malaria control interventions also transferred from vectorial controls such as IRS, ITNs combined with case management to enhancing case detection with health education particularly on risk and vulnerable population. Considering the complication and uncertain quality of social and economical factors only the geographical environment and biological factors were analysed to determine the key factors related to the malaria outbreak and re-emergence, which would help to formulate methodologies for malaria monitoring, forecasting and early warning.
Discussion
As with other vector-borne diseases, malaria typically was driven by climatic, ecological and human factors [
11‐
15]. Previous studies [
16‐
18], focused on the
Anopheles flavirostris and
Anopheles gambiae, had found a negative relationship between the risk of malaria infection and the distance from the
Anopheles breeding sites to the houses. Entomological surveys found that the female
Anopheles requires surface water in which to lay her eggs and in which the larvae hatch after 2-3 days.
Anopheles gambiae was observed to breed more prolifically in temporary and turbid water bodies, such as those formed by rain, whereas in permanent water bodies predation becomes important. In studies conducted in the area along the Huang and Huai Rivers,
An. sinensis was the major vector of malaria, with larval habitats in small water-bodies, such as ponds, paddy fields or gullies [
19,
20]. The results of the present study showed the distances from household of cases to the nearest water-body were positive-skew distributed, the median was 60.9 m and people living in the extent of 60 m near to the water-body had more risk of malaria infection than the farther people. Therefore, it could be suggested to identify the targeted high-risk population and strengthen the treatment to mosquito breeding sites.
Spearman correlation showed that monthly incidence of malaria to various monthly climatic variables and T
mean0 and T
mean01 were key factors which had positive correlation to monthly malaria incidence, the correlation coefficients (
r) were 0.447 and 0.453 (
P < 0.01), respectively. The multiple regressions showed that 75.3% changes of monthly malaria incidence contributed to T
mean, T
mean01, R
mean. It has been investigated [
18‐
21] that temperature and rainfall played the determinant role of environmental factors in the transmission of malaria Temperature and rainfall may not influence the transmission of malaria in a linear and direct way. The rainfall often leads to small puddles serving as mosquito breeding sites and it increases humidity, which enhances mosquito survival [
22,
23]. However, the relationship between mosquito abundance and rainfall was non-linear.
The Huang-Huai River region is a stable vectorial area and the severe malaria epidemics in last century were mainly caused by
An. anthropophagus with higher vectorial capacity. However, malaria outbreaks and re-emergence this time was only in areas with
An. sinensis, with 94.2% of malaria cases found in this area, which may indicate that the vectorial capacity of
An. sinensis is increasing. In the past,
An. sinensis was not an effective transmission vector and malaria incidence absolutely depended on the vectorial capacity and infection source [
24]. The vectorial capacities of An. sinensis of two sites were 0.6969 and 0.4689, which were 4.12 and 2.78 times higher compared to that of 1990s [
8,
25]. Transmission potential may be quantified based upon the basic reproduction rate (
R0) of the parasite.
R0 is defined as the average number of successful offspring that the parasite was intrinsically capable of producing. It was expressed as the average number of secondary infections produced from one infected individual introduced into a non-immune host population. The average basic reproduction rate determines endemicity. For the parasite to survive successfully
R0 must be greater than 1;
R0 values of less than 1 indicate diminishing disease risks and a tendency toward unstable conditions [
9].
R0 values of Huaiyuan County and Yongcheng County were 2.16 and 1.45, respectively, which were greater than 1. In recent years, biological barriers, such as cows and pigs, decreased dramatically, which lead to increasing man-vector contacts and increased transmission rates of
An. sinensis.
Socio-economic and housing factors also played an important role in malaria transmission, including the presence of open eaves or the lack of ceilings, population density and the presence of animal close to the house, education and available income in household. In this study, these socio-economic factors were not taken into account. Besides, it was acknowledged that there were likely to have been imperfections in the data given that they were obtained from a passive surveillance system. According to a 2003 national report, it was estimated that only 1/18 (5.6%) cases in China were notified [
4] and malaria diagnosis was also imperfect, and most of malaria cases were diagnosed based on clinical symptoms.
These findings should be considered in future malaria prevention and control projects, especially in malaria outbreak and re-emergence areas. In 2009, an action plan for malaria elimination was proposed by the Ministry of Health in China. Therefore, it is important for the authorities to know how to distribute limited resources effectively.
Competing interests
The authors declare that they have no competing interests.
Authors' contributions
SSZ was responsible for the overall study and the grant from the Ministry of Science, and involved in all stages of this study including design, field work, data analysis and writing manuscript. FH was the focal point in this study and involved in field work and data analysis and wrote the manuscript. SSZ analyzed the relationship between the residence of malaria cases and the water body. JJW and YPS performed to collect malaria incidence data in study sites. All authors read and approved the final manuscript.