Epidemiologic features of overseas imported malaria in the People's Republic of China
- Zhongjie Li†1,
- Qian Zhang†1,
- Canjun Zheng†1,
- Sheng Zhou1,
- Junling Sun1,
- Zike Zhang1, 2,
- Qibin Geng1, 3,
- Honglong Zhang1,
- Liping Wang1,
- Shengjie Lai1, 4,
- Wenbiao Hu5,
- Archie C. A. Clements6,
- Xiao-Nong Zhou7Email author and
- Weizhong Yang8Email author
© Li et al. 2016
Received: 5 December 2015
Accepted: 23 February 2016
Published: 5 March 2016
With the dramatic increase in international travel among Chinese people, the risk of malaria importation from malaria-endemic regions threatens the achievement of the malaria elimination goal of China.
Epidemiological investigations of all imported malaria cases were conducted in nine provinces of China from 1 Nov, 2013 to 30 Oct, 2014. Plasmodium species, spatiotemporal distribution, clinical severity, preventive measures and infection history of the imported malaria cases were analysed using descriptive statistics.
A total of 1420 imported malaria cases were recorded during the study period, with P. falciparum (723 cases, 50.9 %) and P. vivax (629 cases, 44.3 %) being the two predominant species. Among them, 81.8 % of cases were in Chinese overseas labourers. The imported cases returned from 41 countries, mainly located in Africa (58.9 %) and Southeast Asia (39.4 %). About a quarter (25.5 %, 279/1094) of counties in the nine study provinces were affected by imported malaria cases. There were 112 cases (7.9 %) developing complicated malaria, including 12 deaths (case fatality rate: 0.8 %). Only 27.8 % of the imported cases had taken prophylactic anti-malarial drugs. While staying abroad, 27.7 % of the cases had experienced two or more episodes of malaria infection. The awareness of clinical manifestations and the capacity for malaria diagnosis were weak in private clinics and primary healthcare facilities.
Imported malaria infections among Chinese labourers, returned from various countries, poses an increasing challenge to the malaria elimination programme in China. The risk of potential re-introduction of malaria into inland malaria-free areas of China should be urgently addressed.
KeywordsMalaria Imported Epidemiology China
Malaria, transmitted via the bite of infected Anopheles mosquitoes, is one of the most important parasitic diseases to affect mankind with a heavy burden of disease . Globally an estimated 3.3 billion people are at risk of being infected with malaria and developing disease. In 2013, 198 million cases of malaria occurred, leading to 584,000 deaths . Due to joint efforts made by the international community, the global burden of malaria has decreased substantially during recent decades , with a 47 % decline in malaria mortality rates globally, averting an estimated 4.3 million deaths between 2001 and 2013 . In 2015, the World Health Organization (WHO) set an ambitious new target of reducing the global malaria burden by 90 % by 2030, and encouraged nation members to fulfill the goal of malaria elimination .
Malaria is a mandatory notifiable infectious disease in the People's Republic of China, with each case required to be reported through the National Infectious Disease Reporting Information System . Historically, malaria has been the most prevalent infectious disease in P.R.China, accounting for more than 24 million cases during the early 1970s . Long-term implementation of anti-malaria campaigns in areas with high transmission of malaria in P.R.China, including strengthening surveillance systems, improving access to treatment, preventive anti-malarial administration for high-risk groups, environmental improvement, vector control, and social mobilization, has resulted in an unprecedented decrease in number of malaria-endemic areas in mainland China [7, 8]. Autochthonous malaria cases have numbered in only the hundreds annually during the past several years [7–10]. The call for global malaria elimination advocated by WHO was responded actively in P.R.China, with a national malaria elimination action plan being launched by the Chinese central government in 2010, which intends to reach the goal of malaria elimination nationwide by 2020 [11–13]. A challenge is the globalization strategy for economic development in P.R.China, which is resulting in more cases of imported malaria in recent years [14–16]. Of particular concern is the threat to individual health of Chinese citizens travelling abroad, and the potential re-introduction of local transmission in malaria-free areas when travellers return. To facilitate better response strategies for this new challenge, the epidemiological features of imported malaria need to be further explored. In this study, a case-based epidemiological survey on each imported malaria case was conducted in nine provinces of China. The characteristics of importation origin, Plasmodium species, prevention, infection, and clinical outcome of imported malaria are described.
In P.R.China, malaria cases are diagnosed by clinicians in accordance with the unified national diagnostic criteria. Laboratory-confirmed malaria cases refer to patients with any positive result in the following diagnostic tests relating to malaria: malaria parasites confirmed by microscopy, rapid diagnostic tests (RDT), or polymerase chain reaction (PCR) tests. Since the initiation of the National Malaria Elimination Action Plan in 2010, each case should be investigated by local staff at county level of the Centre of Disease Control and Prevention, and each case should be classified as local or imported malaria . A malaria patient is classified as an imported case if the individual travelled to a malaria-endemic country within the previous month . In this study, the last country destination of travel was taken as the origin of malaria infection; a person who went abroad as a member of a group organized by an agency was identified as a group traveller; otherwise a person was identified as an individual traveller.
Background information on the nine study provinces for imported malaria surveys, in China
Population in 2012 (000s)
International travellers in 2012a (000s)
Total malaria cases 2010–2012
Overall of nine study provinces (% of entire country)
584,060 (43.3 %)
61,944.0 (53.3 %)
7296 (52.4 %)
Demographic data, Plasmodium species profiles, spatiotemporal distribution of cases, case detection and clinical features, as well as preventive measures and exposure histories during travel abroad were analysed. A seasonal index was used to understand the seasonal patterns of imported malaria occurrence. An index for a given month (i.e., May) was calculated by case numbers for that month (i.e., May) divided by the monthly mean of cases during the whole 12 months of the survey . No obvious seasonal pattern was expected if the seasonal index of each month was close to 1.0. Medical service providers for malaria diagnosis were categorized by private clinic, primary hospital, hospital at county level, and hospital at city level, according to their population coverage and the techniques, equipment, and staff available.
From 1 Nov, 2013 to 30 Oct, 2014, a total of 1420 imported malaria cases were reported in the study provinces. The mean age of the imported malaria cases was 36.8 years old (range 1–69, IQR 28–45), and 87.4 % (1241 cases) were aged between 21 and 50 years. Males accounted for 95 % of all cases. Overseas labourers were the most frequent occupational group with malaria infection, accounting for 81.8 % of all imported cases.
Plasmodium species by origin and location
P. falciparum (723 cases, 50.9 %) and P. vivax (629 cases, 44.3 %) were the two predominant species. Only 26 P. malariae cases and 31 P. ovale cases were detected. Nine mixed infections were recorded, which included seven cases of P. falciparum mixed with P. vivax, one case of P. falciparum and P. malariae, and one case of P. vivax and P. malariae. The remaining two malaria cases were not sub-typed by species.
The major species of imported malaria varied by sub-region. P. vivax predominated in imported cases returning from Southeast Asia (80.4 %) and eastern Africa (67.5 %), while P. falciparum predominated in cases from western Africa (81.3 %), central Africa (83.1 %), and southern Africa (86.2 %). P. malariae and P. ovale mainly came from central and West Africa (Fig. 1b).
Among the 1094 counties of the nine study provinces, 25.5 % (279 counties) were affected by imported malaria cases. The three leading provinces in terms of numbers of cases were Yunnan (477 cases), Sichuan (249 cases) and Henan provinces (201 cases). In Yunnan Province, three counties that shared land borders with Myanmar were the most severely affected with more than 50 imported cases each. The majority of imported cases (933 cases, 65.7 %) came from non-adjacent countries to China, and the remaining 487 cases (34.3 %) had returned from adjacent countries (Myanmar, Laos, India, and Pakistan).
Case detection and clinical outcome
The detection of imported malaria cases by different health providers in nine provinces of China
Hospitals at county level
Hospitals at city level
Number (%) of initial medical visit
Proportion of cases for whom laboratory testing was done during the initial medical visit % (no. tested/all)
Number (%) of laboratory-confirmed cases
Proportion of cases for whom a travel history was recorded during the initial visit % (no. recorded/all)
Proportion of cases for whom a travel history to malaria-endemic countries was recorded during the initial visit was found to be as high as 95.6 % in patients attending hospitals at city level, but was much lower in private clinic (37.7 %). The median intervals were 2 days (IQR 0–4 days) from symptom onset to first medical visit and 2 days (IQR 0–5 days) from the first medical visit to malaria diagnosis.
Clinical manifestation of imported malaria cases by outpatient and inpatient in nine provinces of China
Overall (n = 1420)
n = 945
n = 475
(n = 389)
(n = 515)
(n = 945)
(n = 334)
(n = 114)
(n = 475)
383 (98.5 %)
514 (99.8 %)
938 (99.3 %)
333 (99.7 %)
113 (99.1 %)
474 (99.8 %)
1390 (97.9 %)
372 (95.6 %)
509 (98.8 %)
920 (97.4 %)
331 (99.1 %)
113 (99.1 %)
470 (98.9 %)
1159 (81.6 %)
282 (72.5 %)
474 (92.0 %)
785 (83.1 %)
248 (74.3 %)
104 (91.2 %)
374 (78.7 %)
1008 (71.0 %)
249 (64.0 %)
423 (82.1 %)
697 (73.8 %)
203 (60.8 %)
90 (78.9 %)
311 (65.5 %)
921 (64.9 %)
234 (60.2 %)
383 (74.4 %)
640 (67.7 %)
188 (56.3 %)
79 (69.3 %)
281 (59.2 %)
414 (29.2 %)
122 (31.4 %)
147 (28.5 %)
281 (29.7 %)
92 (27.5 %)
35 (30.7 %)
133 (28.0 %)
272 (19.2 %)
89 (22.9 %)
85 (16.5 %)
181 (19.2 %)
66 (19.8 %)
22 (19.3 %)
91 (19.2 %)
168 (11.8 %)
42 (10.8 %)
41 (8.0 %)
87 (9.2 %)
44 (13.2 %)
5 (4.4 %)
81 (17.1 %)
112 (7.9 %)
95 (28.4 %)
17 (14.9 %)
112 (23.6 %)
38 (2.7 %)
25 (7.5 %)
25 (5.3 %)
32 (2.3 %)
22 (6.6 %)
1 (0.9 %)
23 (4.8 %)
25 (1.8 %)
23 (6.9 %)
9 (7.9 %)
32 (6.7 %)
Liver function impairment
25 (1.8 %)
38 (11.4 %)
38 (8.0 %)
Acute renal dysfunction
23 (1.6 %)
23 (6.9 %)
23 (4.8 %)
23 (1.6 %)
21 (6.3 %)
4 (3.5 %)
25 (5.3 %)
19 (1.3 %)
17 (5.1 %)
2 (1.8 %)
19 (4.0 %)
7 (0.5 %)
7 (2.1 %)
7 (1.5 %)
5 (0.4 %)
4 (1.2 %)
1 (0.9 %)
5 (1.1 %)
Preventive measures and infection history
Among the 1261 cases (88.8 % of total) who travelled individually or as a part of a group was determined, 738 cases (58.5 %) went abroad as a group, and 523 cases (41.5 %) travelled individually. Of the group travellers, 52.4 % had been trained on malaria prevention measures by the organizing agency. Anti-malarial medication was obtained by 27.8 % of the cases prior to their overseas travel; the figure was 11.3 % among individual travellers. Mosquito repellents were obtained by 40.5 % of patients before travel; the figure was 21.4 % for individual travellers. The overall proportion of bed net usage during the period abroad was 73.4 %. The median period abroad was 157 days; for group travellers, the period was longer (221 days) than for individual travellers (72 days). Nearly half of the cases (50.4 %) had been diagnosed with malaria infection during the period abroad and 27.7 % of the cases had experienced two or more episodes of malaria infection.
This study found that a large number of imported malaria cases were detected in P.R.China, and that overseas labourers were the most frequently affected group. The countries of origin of the infections were widely distributed in Africa and Southeast Asia. Many imported cases presented with complicated symptoms, leading to 12 deaths. The awareness of clinical manifestations and the capacity for malaria diagnosis were weak in private clinics and primary healthcare facilities.
Due to global economic integration and the rapid economic development of China, large numbers of Chinese people travel to malaria-endemic countries for financial investment, commercial trade, labour, and tourism. According to the report from the Chinese Bureau of Exit and Entry Administration, more than 83 million people went abroad to seek job opportunities, travel or study overseas in 2012 . The relationship between the increased economic investment and numbers of exported labourers to Africa from China and the increased number of cases imported has been well established . Overseas labourers engaged in road or bridge building, mining and other outdoor activities are the highest risk group for malaria infection [14–16]. Overseas labourers usually work on construction sites and experience poor living conditions with a lack of access to mosquito control measures. Additionally, Chinese labourers generally lack immunity to local Plasmodium species, especially to P. falciparum in Africa, and exported labourers are generally poorly educated and lack awareness of the risk of malaria and personal protection against mosquito bites . Guidelines on malaria chemoprophylaxis for international travellers should be developed in China, so as to reduce the risk of malaria infection among high-risk groups.
With the widespread occurrence of imported malaria, several threats are now facing China. Firstly, a large number of imported cases were due to P. falciparum, the species most commonly associated with severe disease and death, meaning that prompt diagnosis and appropriate treatment are critical . However, this Plasmodium species was relatively rare in most settings in China, and most healthcare workers at primary level lack awareness and skills to diagnose and manage cases infected with falciparum malaria . Furthermore, a report on one large-scale cluster of imported malaria cases returning from Ghana showed that about 34.4 % of Plasmodium-positive persons had asymptomatic infections , which further complicates timely detection by routine malaria surveillance system. Therefore, it is estimated in this study that nearly 30 % of imported cases were likely under-reported. In addition, whilst most local transmission of malaria in China has been successfully interrupted , wide distribution of A. sinensis throughout the country may make many areas receptive to transmission . As a result, imported vivax malaria may lead to re-introduction in areas that have been free of malaria for many years [26, 27], presenting a threat to nationwide malaria elimination by 2020.
Along with the rapid development of international trade and overseas travel in China, it is expected that the situation of disease importation will become more problematic if effective preventive measures are not undertaken [9, 28]. Malaria infection prevention measures, intensive surveillance and medical service delivery to exported labourers should be prioritized by the Chinese public health authorities [13, 29]. Intersectorial cooperation between public health, medical, commercial, and travel sectors could play a critical role in the prevention, detection and management of imported malaria. Training of local epidemiologists and physicians on malaria case diagnosis and investigation needs to be enhanced. The epidemiological features of imported malaria cases and the impact of imported cases on malaria elimination in China should be further explored with long-term data.
One of the limitations on this study was that, as the survey was retrospectively performed, the information on imported case exposure, infection and treatment history when staying abroad may have some recall bias, given that the travellers had lived and worked overseas for a long time at the time of survey. In addition, as only imported cases diagnosed as malaria were enrolled in this study, the population of travellers returned to China from various countries during the survey period was unavailable, and thereby the incidence of malaria among overseas travellers could not be estimated.
This study shows that overseas infections of malaria have become a major threat to Chinese labourers travelling to countries in West Africa, East Africa, and Southeast Asia. In order to reduce the infection risk of malaria during periods abroad, awareness and effective protective measures against exposure to mosquitoes and malaria parasites among high-risk groups should be enhanced. The need to improve capacity for imported case detection and the timeliness of anti-malarial treatments should be highlighted, so as to reduce burden of severe malaria disease and deaths, as well as prevent secondary malaria transmission within China.
ZL, XZ and WY conceived, designed and supervised the study. ZL, QZ and CZ carried out the study, finalized and interpreted the analysis, and wrote the drafts of the manuscript. ZZ, QG, SZ, JS, SL, HZ, and LW assisted in data collection and analysis. WH and ACC participated in the results interpretation and manuscript revision. All authors read and approved the final manuscript.
We acknowledge staff members of the provincial Centres for Disease Control and Prevention or Parasite Control and Prevention Institution in Liaoning, Gansu, Henan, Shandong, Shanghai, Hunan, Guangdong, Sichuan, and Yunnan provinces of China for their assistance in the field investigation and data collection. This study was supported by grants from the Ministry of Science and Technology of China (2012ZX10004-201, 2012ZX10004-220, 2014BAI13B05) and the Ministry of Health of China (No. 201202006). The sponsor of the study had no role in the study design, data collection, analysis, and interpretation, preparation of the manuscript, or the decision to publish.
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- White NJ, Pukrittayakamee S, Hien TT, Faiz MA, Mokuolu OA, Dondorp AM. Malaria. Lancet. 2014;383:723–35.View ArticlePubMedGoogle Scholar
- World Health Organization. World Malaria Report. Geneva: WHO; 2014. Available at http://www.who.int/malaria/publications/world_malaria_report_2014/en/
- Noor AM, Kinyoki DK, Mundia CW, Kabaria CW, Mutua JW, Alegana VA, et al. The changing risk of Plasmodium falciparum malaria infection in Africa: 2000–10: a spatial and temporal analysis of transmission intensity. Lancet. 2014;383:1739–47.View ArticlePubMedPubMed CentralGoogle Scholar
- World Health Organization. Global Technical Strategy for Malaria 2016–2030. Geneva: WHO. Available at http://www.who.int/malaria/areas/global_technical_strategy/en/
- Wang LD, Wang Y, Jin SG, Wu ZY, Chin DP, Koplan JP, et al. Emergence and control of infectious diseases in China. Lancet. 2008;372:1598–605.View ArticlePubMedGoogle Scholar
- Zhou ZJ. The malaria situation in the People’s Republic of China. Bull World Health Organ. 1981;59:931–6.PubMedGoogle Scholar
- Hsiang MS, Hwang J, Tao AR, Liu Y, Bennett A, Shanks GD, et al. Mass drug administration for the control and elimination of Plasmodium vivax malaria: an ecological study from Jiangsu province, China. Malar J. 2013;12:383.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang SQ, Li YC, Zhang ZM, Wang GZ, Hu XM, Qualls WA, et al. Prevention measures and socio-economic development result in a decrease in malaria in Hainan, China. Malar J. 2014;13:362.View ArticlePubMedPubMed CentralGoogle Scholar
- Feng J, Xiao HH, Xia ZG, Zhang L, Xiao N. Analysis of malaria epidemiological characteristics in the People’s Republic of China, 2004–2013. Am J Trop Med Hyg. 2015;93:293–9.View ArticlePubMedGoogle Scholar
- Zhang Q, Lai SJ, Zheng CJ, Zhang HL, Zhou S, Hu WB, et al. The epidemiology of Plasmodium vivax and Plasmodium falciparum malaria in China, 2004–2012: from intensified control to elimination. Malar J. 2014;13:419.View ArticlePubMedPubMed CentralGoogle Scholar
- National Health and Family Planning Commission of the People’s Republic of China. Action Plan of China Malaria Elimination (2010–2020) (in Chinese). Available at http://www.gov.cn/gzdt/att/att/site1/20100526/001e3741a2cc0d67233801.doc
- Zhou XN, Xia ZG, Wang RB, Qian YJ, Zhou SS, Utzinger J, et al. Feasibility and roadmap analysis for malaria elimination in China. Adv Parasitol. 2014;86:21–46.View ArticlePubMedGoogle Scholar
- Cao J, Sturrock HJ, Cotter C, Zhou SS, Zhou HY, Liu YB, et al. Communicating and monitoring surveillance and response activities for malaria elimination: China’s “1-3-7″ strategy. PLoS Med. 2014;11:e1001642.View ArticlePubMedPubMed CentralGoogle Scholar
- Li Z, Yang YC, Xiao N, Zhou S, Lin KM, Wang DQ, et al. Malaria imported from Ghana by returning gold miners, China, 2013. Emerg Infect Dis. 2015;21:864–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Liu YB, Hsiang MS, Zhou HY, Wang WM, Cao YY, Gosling RD, et al. Malaria in overseas labourers returning to China: an analysis of imported malaria in Jiangsu Province, 2001–2011. Malar J. 2014;13:29.View ArticlePubMedPubMed CentralGoogle Scholar
- Feng J, Yan H, Feng XY, Zhang L, Li M, Xia ZG, et al. Imported malaria in China, 2012. Emerg Infect Dis. 2014;20:1778–80.PubMedPubMed CentralGoogle Scholar
- Chinese Center for Disease Control and Prevention. Technical Scheme of China Malaria Elimination (edition in 2011) (in Chinese). Available at http://www.chinacdc.cn/tzgg/201109/P020110906378403678170.doc
- China National Tourism Administration. The annual statistical bulletin of China’s tourism industry in 2012 (in Chinese). Available at http://www.cnta.gov.cn/zwgk/lysj/201506/t2015061018908shtml
- National Bureau of Statistics of China. National data, 2013 (in Chinese). Available at http://data.stats.gov.cn/easyquery.htm?cn=E0103&zb=A0201%C2%AE=620000&sj=2012
- Xiao D, Long Y, Wang SQ, Wu KJ, Xu DZ, Li HT, et al. Epidemic distribution and variation of Plasmodium falciparum and Plasmodium vivax malaria in Hainan, China during 1995–2008. Am J Trop Med Hyg. 2012;87:646–54.View ArticlePubMedPubMed CentralGoogle Scholar
- Bureau of Exit and Entry Administration of the Ministry of Public Security. The steady growth of the number of international travellers and transport in 2012, China (in Chinese). Available at http://www.cnta.gov.cn/zwgk/lysj/201506/t20150610_18908.shtml
- Zhang M, Liu ZY, He HT, Luo L, Wang SQ, Bu HL, et al. Knowledge, attitudes, and practices on malaria prevention among Chinese international travellers. J Travel Med. 2011;18:173–7.View ArticlePubMedGoogle Scholar
- Wang RB, Zhang J, Zhang QF. Malaria baseline survey in four special regions of northern Myanmar near China: a cross-sectional study. Malar J. 2014;13:302.View ArticlePubMedPubMed CentralGoogle Scholar
- Clements AC, Barnett AG, Cheng ZW, Snow RW, Zhou HN. Space-time variation of malaria incidence in Yunnan province, China. Malar J. 2009;8:180.View ArticlePubMedPubMed CentralGoogle Scholar
- Zhou SS, Huang F, Wang JJ, Zhang SS, Su YP, Tang LH. Geographical, meteorological and vectorial factors related to malaria re-emergence in Huang-Huai River of central China. Malar J. 2010;9:337.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang DQ, Li SG, Cheng ZB, Xiao N, Cotter C, Hwang J, et al. Transmission risk from imported Plasmodium vivax malaria in the China-Myanmar border region. Emerg Infect Dis. 2015;21:1861–4.View ArticlePubMedPubMed CentralGoogle Scholar
- Sleigh AC, Liu XL, Jackson S, Li P, Shang LY, et al. Resurgence of vivax malaria in Henan Province. China. Bull World Health Organ. 1998;76:265–70.PubMedGoogle Scholar
- Yin JH, Yang MN, Zhou SS, Wang Y, Feng J, Xia ZG. Changing malaria transmission and implications in China towards National Malaria Elimination Programme between 2010 and 2012. PLoS ONE. 2013;8:e74228.View ArticlePubMedPubMed CentralGoogle Scholar
- Zhou XN, Bergquist R, Tanner M. Elimination of tropical disease through surveillance and response. Infect Dis Poverty. 2013;2:1.View ArticlePubMedPubMed CentralGoogle Scholar