Background
Malaria is one of the most important parasitic infections in human beings. The condition is caused by infection by one or more of five
Plasmodium species via the bite of infected female
Anopheles mosquitoes [
1,
2]. According to the World Health Organization (WHO) estimates, in 2015, 3.2 billion people were at risk of being infected with malaria and developing the disease, and 214 million cases of malaria and 438,000 deaths occurred globally [
3]. As a result of efforts and progress made by the international community, global malaria incidence decreased dramatically between 2000 and 2010 [
4]. In 2015, the WHO set the ambitious new target of reducing the global malaria burden by 90% by 2030, and it encouraged member states to fulfill the goal of malaria elimination [
5]. However, many countries face challenges in achieving the elimination goal because of the threat of malaria importation and re-introduction [
6], especially in border areas adjacent to high malaria endemic countries. In South Korea, for example, there had been no indigenous malaria cases after 1984, until the re-emergence of
P. vivax in the demilitarized zone showed that malaria transmission along the border of North Korea would continue to be a challenge [
7].
China has had remarkable success in controlling locally transmitted malaria through several initiatives facilitated by increased funding, including: effective vector control, strengthening of health systems, improving case management with more effective treatment regimens, and enhanced case reporting and surveillance [
8]. Since 2010, annual numbers of reported malaria cases have fallen to unprecedentedly low levels, with only hundreds of autochthonous malaria cases now occurring in limited areas [
9‐
11]. In 2010, the Chinese government launched the national malaria elimination programme with the goal of eliminating malaria nationwide by 2020 [
12]. However, China shares more than 22,000 km of land border with 14 neighbouring countries, six of which are still malaria-endemic [
3,
13,
14]. Malaria from these countries, especially Myanmar poses a major threat to the achievement and maintenance of national malaria elimination [
15]. Although there were checks in international land borders, population movement between China and other malaria-endemic countries becoming even more frequent was still a high risk of malaria infection. The epidemiological situation in these high-risk areas needs to be further investigated. In this study, the changing risk of malaria occurrence in all counties with international land borders was explored following the initiation of the Chinese malaria elimination programme in 2010, in order to identify remaining high-risk areas, formulate response measures and allocate resources for malaria elimination.
Discussion
This study found that the magnitude and geographic distribution of malaria in the international land border counties of China decreased dramatically since the initiation of the malaria elimination programme in 2010. There has been a lot more imported malaria than indigenous malaria in these regions.
Regional diversity affects the epidemiological characteristics of malaria in the land border regions in northern, western and southern China. In northern and western China, including Inner Mongolia, Xinjiang, Gansu, Heilongjiang and Jilin provinces, low population density and climate are not conducive to the transmission of malaria. Therefore, few local malaria cases were confirmed in these provinces. Moreover, the neighbouring countries of these provinces are generally low-transmission settings. The WHO categorizes Mongolia, Russia and Kazakhstan as malaria-free countries, and they present almost no risk of introducing malaria into China [
22].
Nevertheless, in Liaoning province, indigenous malaria recently emerged in Dandong city. Dandong city is close to the border with North Korea, with frequent movement of people and goods across the border, and mosquito vectors capable of malaria transmission [
23‐
26]. Currently, the risk of malaria spreading from North Korea to China is hard to estimate, because the epidemic situation in North Korea is uncertain [
3].
In Motuo county of Tibet, the local humid and sub-tropical monsoon climate is suitable for mosquitoes breeding. Because it is a remote area, healthcare services have difficulty reaching the local population [
27]. In order to achieve the nationwide elimination goal, malaria prevention and treatment should be prioritized in such hard-to-reach areas.
There were most reported malaria cases in Yunnan province, and the adjacent countries of Yunnan were in the controlling malaria stage. Hence, Yunnan province was further focused on. Several counties in Yunnan with persistent indigenous malaria cases, especially along the border with Myanmar, pose the greatest threat to achieving national malaria elimination [
28]. However, it is encouraging that malaria in the land border regions of Yunnan province was effectively controlled in recent years by joint and cross-border prevention and control strategies. Indigenous transmission of malaria has been interrupted in many regions. The strategies used include timely detection, diagnosis and appropriate treatment for malaria cases; finding the source of infection promptly in all land border counties; setting up malaria prevention stations in the border points; and active screening in exported labour to reduce the spread of malaria out of China [
29‐
31].
Nevertheless, indigenous malaria cases still consistently occurred in several land border counties during this study. The border of Yunnan province is nearly 4060 km, with 18 border ports and 643 border pathways. Because Yunnan province has the highest border region population density, frequent cross-border travel and difficulty managing the migrant population, prevention and control of malaria a more complex [
32,
33]. The key Challenges of elimination by 2020 are mainly related to cross-border and imported malaria. Therefore, more sensitive and quicker responses for case identification are necessary. Village-level capacity for malaria diagnosis, treatment and county-level surveillance and management of exported labour should be strengthened to prevent local secondary malaria case occurrence [
34]. International collaborations as the Asia Pacific Malaria Elimination Network, the Asia Pacific Leaders Malaria Alliance and China’s Belt and Road Initiative need to be further enhanced for the control of imported malaria.
This study only focused on malaria risk in land border regions, because China has long land borders and some neighbouring countries are highly-endemic for malaria. However, in today’s world, malaria can be imported through air and sea transportation, and this could also potentially reintroduce local transmission in areas in the interior with conditions conducive to malaria transmission. For example, a large outbreak of imported malaria occurred in 2013 in Shanglin county, the inner county of Guangxi autonomous regions, which arose from Chinese gold miners returning from overseas (30). Further study of malaria importation and reintroduction should occur in regions with concentrated air and sea transportation and high levels of tourism.
Authors’ contributions
QZ and ZL conceived, designed and supervised the study. QZ, JS and ZZ carried out the study, finalized and interpreted the analysis, and wrote the drafts of the manuscript. QG assisted in data collection and analysis. SL, WH and ACC participated in the results interpretation and manuscript revision. All authors read and approved the final manuscript.