Emerg Infect DisEmerging Infect. DisEIDEmerging Infectious Diseases1080-60401080-6059Centers for Disease Control and Prevention25279813419318014-059510.3201/eid2010.140595Letters to the EditorLetterImported Malaria in China, 2012Imported Malaria in China, 2012Imported Malaria in China, 2012FengJun1YanHe1FengXin-yuZhangLiLiMeiXiaZhi-guiXiaoNingAddress for correspondence: Ning Xiao, National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of Health, World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, 207 Rui Jin 2 Rd, Shanghai 200025, China; email: ningxiao116@126.com102014201017781780Keywords: malariaimported malariaparasitesPlasmodium speciesworkersChina

To the Editor: Imported malaria has become a major public health challenge in China. Despite an 89.8% decrease in total cases from 2008 (26,873) through 2012 (2,729), the proportion of imported malaria cases has increased from 14.7% to 89.0% (1). We analyzed the malaria situation in China in 2012 by using data obtained from the national information reporting system of infectious diseases.

In this analysis, an imported case of malaria was defined as case of malaria acquired in a known malarious area outside China. In China, the following criteria for imported malaria must be simultaneously met: 1) the patient was given a diagnosis of malaria; 2) the patient had a travel history to malaria-endemic areas outside China during malaria transmission season; and 3) the onset time for malaria for the person was <1 month after returning to China during the local transmission season. This definition of malaria was based on the latent period for all Plasmodium species reported in China.

Of 2,729 malaria cases reported in 2012, a total of 2,428 (89.0%) were imported. Fifteen of these cases were in persons who died of infection with P. falciparum. In the imported cases, 4 Plasmodium species were identified: P. falciparum (n = 1,423 [58.6%]), P. vivax (n = 909 [37.5%]), P. ovale (n = 42 [1.7%]), P. malariae (n = 20 [0.8%]), and mixed infections (n = 21 [0.9%]). Among imported cases, 13 (0.5%) were clinically diagnosed.

Chinese workers who returned from Africa (n = 1,458 [60.0%]) had most cases imported malaria. A total of 37 countries in Africa were sources of imported cases. Most cases were acquired in Ghana (n = 241 [9.9%]), Equatorial Guinea (n = 233 [9.6%]), and Nigeria (n = 197 [8.1%]). Case-patients were predominantly infected by P. falciparum (n = 1,187 [81.4%]). Southeast Asia (n = 895 [36.9%]), including Myanmar (n = 764 [31.5%]), Cambodia (n = 49 [2.0%]), and Laos (n = 36 [1.5%]), was another major source of imported cases. These case-patients were infected mostly with P. vivax (n = 658 [73.5%]) (Table).

Malaria cases imported into China from other countries, by country and <italic>Plasmodium</italic> species, 2012
Country of originTotal, n = 2,428, no. (%)Species, no. (%)
P. falciparum, n = 1,423P. vivax, 
n = 909P. malariae, n = 20P. ovale, 
n = 42Mixed, 
n = 21Unclassified, n = 13
Africa1,458 (60.0)1,187 (83.4)192 (21.1)16 (80.0)40 (95.2)12 (57.1)11 (84.6)
Ghana241207214234
Equatorial Guinea2331872521531
Nigeria197172191500
Angola151127134502
Guinea605630100
Sudan5034160000
Liberia4532101110
Republic of Congo433441220
Sierra Leone423630111
Gabon373140200
Democratic Republic of Congo362860110
Ethiopia309210000
Mozambique201820000
Cameroon181260000
Côte d’Ivoire171700000
Mali171520000
Tanzania171520000
Zambia161510000
Uganda161140100
South Sudan161600000
Chad11830000
Malawi10810100
Central African Republic8701000
South Africa8421100
Senegal5410000
Benin5410000
Burkina Faso5500000
Kenya5410000
Madagascar5500000
Niger4400000
Libya3120000
Zimbabwe2200000
Togo2200000
Rwanda2110000
Mauritania1010000
Egypt1100000
Algeria1010000
Unknown
78
55
16
1
2
1
3
Southeast Asia895 (36.9)224 (15.7)658 (72.4)3 (15.0)1 (2.4)9 (42.9)0
Myanmar7641985572160
Cambodia491461010
Laos364320000
Indonesia3517160020
East Timor3030000
Vietnam5320000
Thailand1010000
Malaysia1100000
Unknown
1
0
1
0
0
0
0
Southern Asia45 (1.8)4 (0.3)39 (4.3) 01 (2.4)01 (7.7)
Pakistan294240100
India140130001
Afghanistan
2
0
2
0
0
0
0
Eastern Asia2 (0.1)02 (0.2)0000
South Korea1010000
North Korea
1
0
1
0
0
0
0
Oceania6 (0.2)2 (0.2)4 (0.5)0000
Papua New Guinea
6
2
4
0
0
0
0
Latin America1 (0.1)01 (0.1)0000
Brazil
1
0
1
0
0
0
0
Unknown21 (0.9)6 (0.4)13 (1.4)1 (5.0)001 (7.7)

Imported cases increased during April, reached a peak during May (n = 297 [12.2%]), and decreased during July. This trend was caused by workers returning to China to perform agricultural work during this period. The male:female patient ratio was 14.6:1 (n = 2,272 male patients:156 female patients); most (n = 2,240 [95.2%]) mobile laborers are men. The mean age of persons with imported cases was 40.8 years. Most (n = 1,813 [74.7%]) of these persons were 15–44 years of age and few (n = 5 [0.2%]) were <5 years of age.

Persons with imported cases were detected in 29 provinces (Hong Kong, Macao, and Taiwan did not join the information system). Yunnan (n = 690 [28.4%]), Guangxi (n = 209 [8.6%]), and Jiangsu (n = 197 [8.1%]) Provinces had the largest number of imported cases.

Our analysis indicated that imported malaria poses major challenges to the malaria elimination program in China. One challenge is the increasing investment in overseas work and increasing numbers of Chinese persons who are working abroad. The total number of Chinese laborers and travelers abroad in 2012 was estimated to be 0.5 million and 83.2 million persons, respectively; these numbers increased by 24.6% and 44.9%, respectively, from numbers in 2010. Another reason for the increasing proportion of imported malaria cases was a sharp decrease in locally acquired infections. There were only 246 locally acquired cases in 2012, a decrease of 94.2% from the number of locally acquired cases in 2010 (2).

Because imported malaria is widely distributed throughout China, the disease could be introduced into malaria-free localities during the transmission season, especially when a large number of cases are clustered in areas in which Anopheles species mosquitoes are prevalent. Additional studies are needed to determine the susceptibility of Anopheles species mosquitoes in China to Plasmodium species that cause human malaria.

In summary, imported malaria poses a severe threat to the malaria elimination program in China (3). For effective management of imported malaria, surveillance systems need to be carefully planned and well managed to ensure timely recognition and prompt response. Effective mechanisms of multisectoral coordination and cooperation should be established and strengthened. In addition, health education information on malaria risks and protection should be provided to all mobile laborers and other travelers before their traveling abroad and after returning home. Labor and travel agencies should provide travelers with essential preventive measures. This information should also be provided to entry and exit border stations and to local Centers for Disease Control and Prevention so that timely malaria tracking can be implemented. Training should also be provided to physicians to ensure provision of accurate diagnosis and appropriate treatment. For local health agencies, prompt case verification and response are required to ensure elimination of residual potential reservoirs and prevention of local transmission caused by imported pathogens.

Suggested citation for this article: Feng J, Yan H, Feng X, Zhang L, Li M, Xia Z, et al. Imported malaria in China, 2012 [letter]. Emerg Infect Dis [Internet]. 2014 Oct [date cited]. http://dx.doi.org/10.3201/eid2010.140595

Acknowledgments

We thank staff members of provincial and county Centers for Disease Control and Prevention in China for assistance.

This study was supported by the China-UK Global Health Support Programme.

National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, China;

MOH Key Laboratory of Parasite and Vector Biology, Shanghai;

World Health Organization Collaborating Centre for Malaria, Schistosomiasis and Filariasis, Shanghai

These authors contributed equally to this article.

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