Trends of imported malaria in China 2010–2014: analysis of surveillance data

Malaria incidence in China has been decreasing since 2010, and this study presented results on a changing malaria situation in China. Historically, P. vivax has been the predominant Plasmodium species in China, varying from 77 to 94 % annually between 2001 and 2009. The relative proportions of falciparum and vivax malaria cases have reversed between 2010 and 2014, and currently P. falciparum is the predominant species of all malaria cases (autochthonous and imported) in China. The changing proportion of Plasmodium malaria has been mainly due to effective malaria control activities nationwide. Moreover, the total proportion of P. ovale and P. malariae cases increased during this period. As of 2014, the only remaining autochthonous malaria cases were identified in Yunnan and Tibet provinces, with Yunnan being the last stronghold for ongoing P. falciparum malaria transmission.

Imported malaria cases had different characteristics compared to autochthonous malaria cases. Autochthonous malaria cases were typically identified among all age groups, originated in specific endemic areas, and during clear seasonal peaks. Major characteristics of imported cases included being adult, male, and farming as an occupation with reported labour-related travel history to other countries. Additional characteristics of imported cases included being reported in the non-transmission season, and were distributed nationwide, even in the areas with no history of malaria transmission [16‐19]. This is a challenge for passive surveillance systems in those counties or provinces currently without malaria transmission because of their poor capacity of case detection as total malaria incidence reduces to zero in many counties. Maintenance of case detection in certain health facilities should be a critical activity where surveillance was taken as one intervention during malaria elimination in China.

Between 2010 and 2014, imported P. falciparum was reported in all provinces in China, largely due to importation from other countries, especially from Africa where P. falciparum is the main parasite. This may be partly attributed to an increasing number of Chinese labourers who visit Africa given the recent cooperation between Africa and China. Tatem et al. indicated that certain countries in West African and Central Asia are more strongly connected by high levels of infection movement than others [20]. This study found that 94 % of imported cases had recent labour-related travel history. Similarly, Liu et al. indicated that imported malaria cases in Jiangsu Province, China were mostly related to the export of labour [21]. Statistics from the China Ministry of Commerce shows that legal export of labour overseas included approximately 800,000 individuals annually over the past 5 years and the number of export labourers continues to rise each year [22]. Given this trend, international population movement between China and other malaria-endemic countries will be become even more frequent. The study findings presented the diversity of malaria importation from both African and Asian countries. Ninety percent of imported falciparum malaria came from African countries thereby increasing the chance of potentially fatal cases [9]. Intervention regarding malaria among this internationally moving population should be undertaken. Malaria intervention in the border areas should be strengthened.

Compared to those travelling for tourism or business, overseas labourers stayed for longer periods, which possibly contributed to an increased risk of contracting malaria. Study findings support the targeting of malaria prevention activities in these higher risk groups. To reduce the burden of imported malaria cases in Chinese workers coming from other countries after long stays, interventions should be specific Chinese export labourers. Within this high burden group, evidence has shown there is poor knowledge and awareness of malaria prevention methods [23, 24]. Chemoprophylaxis alone may not be a good choice due to poor understanding of benefit of taking prophylaxis and the potential negative side effects, such as resistance to anti-malarial drugs. Given the increase in numbers of overseas labourers, the supply of chemoprophylaxis in these groups would also be a challenge. Chinese export labourers work mostly in construction and mining activities, therefore, occupation-based vector control methods should be considered [25, 26], including specific behaviour change communication activities.

Furthermore, the seasonal distribution of imported malaria into China fluctuated very little. However, within four to 5 weeks, 874 imported malaria cases in 2013 were detected after 4052 Chinese gold miners returned to China after working in Ghana [27]. This event indicated that timely detection and removal of new infections is critical to prevent re-establishment of transmission [28].

This study’s findings show that 15 % of imported P. falciparum cases and 60 % of imported P. vivax cases had symptoms more than 30 days after returning from abroad. On the one hand, it indicated the definition of imported malaria should be revised. During the malaria control phase, travel history within the previous month is an appropriate definition to determine imported malaria. However, in the malaria elimination phase, the definition of imported malaria must include up to 3 months of travel history. On the other hand, it also indicated those cases should be identified as early as possible by active case detection, including reactive case detection and proactive case detection [26].

To conduct effective surveillance in this malaria elimination setting, new strategies and activities are needed. Although total malaria incidence is decreasing in China, highly sensitive diagnostics (such as PCR/LAMP) that are field-friendly, as well as genotyping techniques, are needed to identify asymptomatic and sub-patent infections and to distinguish the origin of those infections [29]. With improved rapid reporting capacity and targeted active and passive surveillance activities, responding to imported cases should be greatly improved among the target population at risk after returning from malaria-endemic countries [30, 31].

Study limitations should be mentioned. National surveillance data in China are routinely collected using standardized forms. However, some missing epidemiological data were identified in ISPDCP due to a loss-to-follow-up after treatment in the health facility. Since ISPDCP was established in late 2011, malaria case investigation data collected prior to this starting were subsequently added to the ISPDCP database. Therefore, data in 2010 and 2011 may not be a reliable source of autochthonous cases, especially in some geographic areas of China. For example, the rate of missing case classification of case investigation was 17 % from 2011 to 2014. However, the ISPDCP database is the best source for national level data in China and there is no evidence to suggest that malaria cases with missing travel history information were systematically different than those with complete reports. Further, this study presented data showing that the quality of the malaria case information captured in the surveillance system has improved over the study period. Both imported and autochthonous malaria cases may be underestimated in 2010 and 2011 due to misclassification bias. In those provinces that have eliminated falciparum malaria, the identification of the parasite may be easier once travel history to endemic areas is considered. However, China’s border areas with Laos, Myanmar and Vietnam make it more difficult to ascertain imported malaria. For example, 74 % of these cases reported in 2010 had an unknown origin of infection. Since China began to pursue malaria elimination in 2010, improvements to the epidemiological survey form have been made and information collection improved. New factors were included in the revised case investigation forms, namely the origin of infection. The missing rate of origin of infection improved since 2011 and was only 1 % of the total in 2014. Another limitation was the result from current definition of case classification in China: 23 % of total imported cases with missing infection locations were partly due to the definition.