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. 2020 Apr 24;2(17):277–283.

Imported Malaria Cases — China, 2012–2018

Jun Feng 1,&, Hong Tu 1,&, Li Zhang 1, Zhigui Xia 1, Shuisen Zhou 1,*
PMCID: PMC8422169  PMID: 34594639

ABSTRACT

Introduction:In 2017, no indigenous malaria cases were reported in China, but imported malaria was a challenge for the elimination program. This study analyzed the status and trends of imported malaria in China from 2012 to 2018 to provide evidence for further strategies and adjustments to current interventions.

Methods: Data on individuals were collected from the Parasitic Diseases Information Reporting Management System (PDIRMS) from 2012 to 2018. Plasmodium species, case classification, temporal distribution, spatial distribution, and source of imported cases were analyzed to investigate imported malaria characteristics.

Results:In total, 21,376 malaria cases were recorded in the PDIRMS from 2012 to 2018. Among them, 20,938 (98.0%) cases were imported malaria cases (IMCs). The number and proportion of IMCs increased from 2012 (n=2,474, 91.0%) to 2018 (n=2,511, 99.7%). IMCs consisted of 13,510 (64.5%) P. falciparum, 4,803 (22.9%) P. vivax, 1,725 (8.2%) P. ovale, 376 (1.8%) P. malariae, 2 (0.01%) P. knowlesi, 348 (1.7%) mixed infections, and 174 (0.8%) clinically-diagnosed cases. The proportion of imported P. falciparum cases increased from 2012 (n=1403, 57.4%) to 2018 (n=1655, 66.0%), while imported P. vivax cases showed a decreasing trend from 2012 (n = 901, 43.7%) to 2018 (n=352, 14.0%). IMCs were mainly reported in Yunnan (n=2,922, 14.0%), Guangxi (n=2,827, 13.5%), and Jiangsu (2,067, 9.9%). IMCs were reported throughout the entire year, and the highest number of IMCs was reported in June 2013. IMCs originated from 67 countries from 4 continents, and the largest proportion were from Myanmar (n=3,081, 14.7%) and Ghana (n=2,704, 12.9%).

Conclusion and Implications for Public Health Practice: The total number of IMCs increased in China. Therefore, two actions are needed to continue the elimination of malaria in China: prevent re-establishment caused by imported P. vivax because Anopheles sinensis is still widely distributed; and ensure timely diagnosis and appropriate treatment to avoid fatal cases caused by imported P. falciparum.

INTRODUCTION

China has succeeded in controlling indigenous malaria and has reached milestones towards malaria elimination since the National Malaria Elimination Action Plan has launched in 2010 (1-3). In 2017, for the first time, no indigenous cases were reported in China (4). However, with increasing globalization, larger numbers of people go to or return from malaria endemic areas and present challenges to malaria elimination in China (5).

Imported malaria cases (IMCs) may increase risks in malaria-free localities where Anopheles mosquitoes still exist. In addition, severe malaria infections caused by Plasmodium falciparum are catastrophic if diagnosis and treatment are not timely.

In 2012, the Parasitic Diseases Information Reporting Management System (PDIRMS) was set up to determine whether every case was indigenous or imported. Therefore, the objective of this study was to characterize the epidemiological status and trends of IMCs from 2012 to 2018 to provide evidence-based data to support the adjustment of appropriate strategies and activities towards the achievement of malaria elimination not only in China but also in other countries with similar elimination processes.

METHODS

Data from 31 provincial-level administrative divisions (PLADs) were collected via the PDIRMS from 2012 to 2018 and carefully reviewed. Plasmodium species, case classification [indigenous①, imported②, or other (induced③, introduced④, relapse⑤ or recrudesce⑥)], and source of imported cases were analyzed to explore the characteristics of IMCs. Clinically-diagnosed cases⑦ and laboratory-confirmed cases⑧ were included in this analysis. Data from Hong Kong, Macao, and Taiwan were excluded from the study. Moreover, data from foreign nationals were not concluded. Statistical analysis was performed using the chi-square test for trends by software SPSS ( version 21.0, IBM Corp., New York, US), and p < 0.05 was considered statistically significant.

RESULTS

In total, 21,376 malaria cases were recorded in the PDIRMS from 2012 to 2018. Among them, 20,938 (98.0%) cases were IMCs. The number and proportion of IMCs increased from 2012 (n=2,474, 91.0%) to 2018 (n=2,511, 99.7%) with statistical significance (evaluated by chi-square test for trends, χ2 = 435.423, p < 0.001). IMCs consisted of 20,764 laboratory-confirm cases and 174 clinically-diagnosed cases. The laboratory-confirmed cases consisted of 13,510 (64.5%) P. falciparum cases, 4,803 (22.9%) P. vivax cases, 1,725 (8.2%) P. ovale cases, 376 (1.8%) P. malariae cases, 2 (0.01%) P. knowlesi cases, 348 (1.7%) mixed infection cases (Table 1). Among these cases, the proportion of imported P. falciparum cases increased from 2012 (n=1,403, 57.4%) to 2018 (n=1,655, 66.0%), while imported P. vivax cases decreased from 2012 (n=901, 43.7%) to 2018 (n=352, 14.0%). In addition, imported P. malariae and P. ovale cases also increased during the same timeframe. In 2012, the proportion of P. malariae and P. ovale cases was 2.3% (n=56), while in 2018, this proportion peaked at 18.0% (n=453). Most IMCs were male (n=19,877, 94.9%), and 1,061 cases (5.1%) were female. The highest number of IMCs was observed in the age group of 46 to 50 years, and most IMCs occurred in migrant workers (n=14,300, 68.3%).

Table 1. Clinically-diagnosed and laboratory-confirmed imported malaria cases in China (2012–2018).

Year Subtotal Laboratory-confirmed cases Clinically-diagnosed cases
P. vivax P. falciparum P. ovale P. malariae P. knowlesi Mixed
* The number of imported P. ovale and P. malariae was not counted separated, so herein we provide the total number of P. ovale and P. malariae.
2012 2,474 901 1,403 56* 0 0 39
2013 4,042 859 2,899 133 51 0 65 35
2014 3,022 798 1,876 231 53 1 44 19
2015 3,077 779 1,895 266 65 0 55 17
2016 3,139 622 2,066 315 64 0 59 14
2017 2,672 496 1,716 350 65 1 35 9
2018 2,511 348 1,655 374 78 0 51 5
Total 20,938 4,803 13,510 1,725 376 2 348 174
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IMCs were mainly reported in the PLADs of Yunnan (n=2,922, 14.0%), Guangxi (n=2,827, 13.5%), and Jiangsu (n=2,067, 9.9%) (Table 2). The distribution of IMCs broadened with cases reported in 618 counties in 2012 and 688 counties in 2018. The temporal distribution showed that IMCs were reported throughout the entire year, and the highest number of IMCs was reported in June 2013 (n=857) (Figure 1).

Table 2. Imported malaria cases in 31 provincial-level administrative divisions (PLADs) in China (2012–2018).

PLADs Total cases Imported cases Proportion of imported cases (%) in the whole country
Number Proportion (%)
Yunnan 3,285 2,922 88.9 14.0
Guangxi 2,828 2,827 99.9 13.5
Jiangsu 2,070 2,067 99.9 9.9
Sichuan 1,697 1,697 100.0 8.1
Henan 1,285 1,285 100.0 6.1
Shandong 1,283 1,282 99.9 6.1
Zhejiang 1,241 1,241 100.0 5.9
Guangdong 1,038 1,035 99.7 4.9
Hunan 969 964 99.5 4.6
Hubei 884 875 99.0 4.2
Anhui 876 845 96.5 4.0
Fujian 637 637 100.0 3.0
Beijing 561 561 100.0 2.7
Shannxi 424 424 100.0 2.0
Liaoning 355 353 99.4 1.7
Hebei 323 323 100.0 1.5
Jiangxi 304 304 100.0 1.5
Shanghai 284 284 100.0 1.4
Chongqing 209 209 100.0 1.0
Gansu 162 162 100.0 0.8
Guizhou 150 150 100.0 0.7
Jilin 105 105 100.0 0.5
Shanxi 93 93 100.0 0.4
Hainan 81 80 98.8 0.4
Tianjin 62 62 100.0 0.3
Heilongjiang 41 41 100.0 0.2
Xinjiang 37 37 100.0 0.1
Ningxia 29 29 100.0 0.1
Inner Monglia 19 19 100.0 0.1
Qinghai 14 14 100.0 0.1
Tibet 30 9 30.0 0.0
Total 21,376 20,936 97.9 100.0
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Figure 1.

Figure 1

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Temporal distribution of imported malaria cases in China (2012–2018).

IMCs originated from 67 countries from 4 continents, and among them, 16,720 cases (79.9%) originated from Africa, mainly central and western Africa, which accounted for 33.5% (n=7,007) and 32.5% (n=6,806) of all IMCs, respectively. IMCs from Africa in this time period showed an increasing trend with 58.8% in 2012 (n=1,454) and 90.4% in 2018 (n=2,470). The imported P. falciparum cases from Africa also showed an increasing trend. In 2012, 32 African countries reported 1,177 P. falciparum cases, while in 2018, 35 African countries reported 1,641 P. falciparum cases. The cases imported from Africa were mainly from Ghana (n=2,704, 12.9%), Angola (n=2,085, 10.0%), and Nigeria (n=1,939, 9.3%) (Table 3).

Table 3. Source of imported cases reported in China (2012–2018).

Regions Country 2012 2013 2014 2015 2016 2017 2018 Total
Africa 1,454 3,243 2,295 2,487 2,689 2,282 2,270 16,720
Southeast Africa 196 311 380 457 541 436 395 2,716
Ethiopia 38 62 118 150 148 113 95 724
Mozambique 22 48 68 75 84 103 104 504
Uganda 16 28 28 53 139 66 41 371
Tanzania 13 34 41 52 49 46 58 293
Sudan 63 72 44 44 7 15 10 255
Zambia 17 37 42 48 47 30 33 254
Kenya 7 6 11 9 14 23 13 83
Malawi 9 9 10 6 11 13 13 71
Madagascar 5 3 9 9 4 8 7 45
South Sudan 0 1 2 3 20 9 10 45
Rwanda 2 2 5 6 14 5 5 39
Zimbabwe 2 3 2 1 2 3 0 13
Djibouti 0 0 0 0 1 2 5 8
Egypt 2 5 0 0 1 0 0 8
Eritrea 0 0 0 1 0 0 1 2
Somalia 0 1 0 0 0 0 0 1
West Africa 641 1,870 879 723 828 950 915 6,806
Ghana 235 1349 188 172 241 347 172 2,704
Nigeria 207 225 341 283 273 286 324 1,939
Guinea 58 75 64 98 72 80 129 576
Côte d’Ivoire 18 16 41 64 104 97 127 467
Liberia 44 86 88 34 39 61 56 408
Sierra Leone 43 55 53 34 43 44 63 335
Benin 5 22 33 10 17 9 12 108
Togo 2 24 50 9 6 4 10 105
Mali 17 14 11 8 10 13 11 84
Burkina Faso 6 3 8 6 3 4 3 33
Niger 0 0 0 1 17 4 3 25
Senegal 5 1 0 2 3 1 4 16
Mauritania 1 0 2 0 0 0 0 3
Gambia 0 0 0 2 0 0 1 3
Central Africa 550 1,038 1,015 1,283 1,292 882 947 7,007
Angola 151 437 272 416 410 192 207 2,085
Equatorial Guinea 247 300 287 272 185 132 115 1,538
Cameroon 17 101 175 248 242 190 159 1,132
Democratic Republic of the Congo 47 64 118 175 244 151 236 1,035
Republic of Congo 33 53 83 101 154 119 98 641
Gabon 35 42 34 43 37 53 73 317
Chad 11 36 38 25 9 13 30 162
The Central African Republic 9 5 5 2 8 28 25 82
Burundi 0 0 3 1 3 4 4 15
South Africa 11 21 17 12 14 9 5 89
South Africa 11 20 15 12 13 8 5 84
Namibia 0 1 1 0 1 1 0 4
Comoros 0 0 1 0 0 0 0 1
North Africa 5 1 0 0 6 4 7 23
Libya 3 0 0 0 5 3 6 17
Algeria 2 1 0 0 1 1 1 6
Africa (Other regions) 51 2 4 12 8 1 1 79
Asia 955 774 706 566 420 359 219 3,999
Southeast Asia 906 736 674 548 392 291 192 3,739
Myanmar 766 605 495 477 326 245 167 3,081
Indonesia 36 71 142 35 27 18 7 336
Laos 37 38 18 12 27 13 5 150
Cambodia 57 19 9 17 6 14 11 133
Vietnam 4 0 3 2 1 1 1 12
Thailand 1 3 5 1 0 0 0 10
Malaysia 2 0 2 2 2 0 0 8
The Philippines 0 0 0 2 3 0 1 6
Timor-Leste 3 0 0 0 0 0 0 3
East Asia 2 1 0 1 1 1 1 7
Democratic People’s Republic of Korea 1 1 0 1 1 0 0 4
Republic of Korea 1 0 0 0 0 1 1 3
South Asia 47 37 32 17 26 67 26 252
Pakistan 31 22 17 10 18 63 22 183
India 14 15 15 7 7 3 4 65
Afghanistan 2 0 0 0 0 0 0 2
Nepal 0 0 0 0 0 1 0 1
Bangladesh 0 0 0 0 1 0 0 1
South America 1 5 2 3 2 10 7 30
Guyana 0 3 2 2 1 6 4 18
Venezuela 0 0 0 1 1 1 3 6
Brazil 1 0 0 0 0 2 0 3
Ecuador 0 1 0 0 0 1 0 2
Surinam 0 1 0 0 0 0 0 1
Oceania 6 8 8 1 16 21 15 75
Papua New Guinea 6 7 8 1 14 19 15 70
Solomon Islands 0 1 0 0 2 2 0 5
Unknown sources 58 12 10 20 13 0 0 113
Total 2,474 4,042 3,021 3,077 3,139 2,672 2,511 20,936
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The cases from another major infection source, namely, Southeast Asia, gradually declined. In this area, 3,999 cases (19.1%) were reported in 2012-2018 with a 77.1% decrease from 2012 (n=955) to 2018 (n=219). In Myanmar, the major source of imported cases in Southeast Asia, the number of P. vivax cases greatly decreased. In 2012, there were 554 P. vivax cases imported from Myanmar, accounting for 22.4% of the IMCs in the same year. In 2018, however, there were only 154 cases imported from Myanmar, accounting for only 6.1% of the IMCs. Moreover, 5 countries from South America and 2 countries from Oceania reported 30 and 75 cases, respectively.

From 2012 to 2018, China reported 111 malaria death cases (0.5%, 111/20,936) among the IMCs, and most of these cases died of P. falciparum infection (n=108, 97.3%), and China also reported 3 unclassified cases. The deaths mainly reported in Sichuan (n=13, 11.7%), Henan (n=12, 10.8%), and Beijing (n=12, 10.8%). The highest number of deaths occurred in 2014 (n=25).

DISCUSSION

For countries that are approaching or have achieved elimination, imported malaria presents a high risk for resurgence or re-establishment (6-7). In 2018, Hunan Province reported 4 introduced cases (P. vivax, first generation), which prompted the Center for Disease Control and Prevention (CDC) staff to strengthen the sensitivity of the surveillance system (8). Since 2012, the proportion of IMCs has increased due to the increased numbers of Chinese workers going to and coming back from abroad. According to data reported by the National Bureau of Statistics of China, the number of migrant workers was 606,000 in 2018, which increased by 16.6% compared to that in 2012 (505,563).

The increasing trend of imported P. falciparum cases from 2012 to 2018 may be explained by the increasing number of migrant workers who travelled to or returned from Africa. The number of imported P. vivax cases increased before 2012 (9) but decreased after 2012. This decreasing trend may have been due to the decline of malaria cases imported from Southeast Asia, especially Myanmar. Several factors have contributed to the reduction of P. vivax in Myanmar. First, the number of P. vivax cases in Myanmar continues to decline, and the number of P. vivax cases decreased from 53,351 in 2007 to 29,944 in 2017 (10-11). Second, Yunnan Province, which neighbors Myanmar, adopted a “three defense line” strategy in the border areas to carry out joint prevention and control with Myanmar to strengthen the surveillance of IMCs (12). Therefore, the number of P. vivax cases reported by the Yunnan Province also declined significantly with a 76.8% reduction from 2012 (599 cases) to 2018 (137 cases). Third, the flow of Chinese nationals changed direction, especially for those in the border areas of Yunnan Province (13).

With regard to the increasing number of P. malariae and P. ovale cases, the increasing number of overseas workers may be one of the factors contributing to this trend as well as the establishment of the provincial reference laboratories. China has established 24 provincial reference laboratories for all the endemic provinces, which have achieved case detection and reconfirmation using polymerase chain reaction and microscopy within 3 day after reporting through the PDIRMS (14). The capacity of the CDC staff to focus on microscopy has strengthened through training by the External Competency Assessment of Malaria Microscopists (ECAMM) held by the World Health Organization (WHO) since 2015. Currently, 19 CDC staff members have obtained first-level certification, and an additional 13 CDC staff members have obtained second-level certification (4).

This study indicated that the number of imported P. vivax cases decreased, while imported P. falciparum cases increased. Therefore, accurate diagnosis and prompt investigation and response need to be strengthened as well as implementation of mobile population-specific measures, especially at the China-Myanmar border to prevent re-establishment caused by imported P. vivax cases (15). Moreover, timely and appropriate treatment by medical staff should be improved to avoid fatal malaria cases caused by imported P. falciparum.

This study is subject to at least a few limitations. First, not all IMCs had exact epidemiological information in 2012−2018. Second, there were 113 unknown cases imported from abroad. Third, not all IMCs were confirmed by laboratory methods as 174 clinically-diagnosed cases were included in this study. Finally, an accurate number of P. ovale and P. malariae cases was not obtained in 2012.

Acknowledgement

We would like to thank the staff members of the provincial and county Centres for Disease Control and Prevention in China for assistance.

Funding Statement

This study was supported by the key techniques in collaborative prevention and control of major infectious diseases in the Belt and Road (2018ZX10101002-004).

Footnotes

Indigenous case: a case contracted locally with no evidence of importation and no direct link to transmission from an imported case. In this study, an indigenous case refers to malaria acquired by mosquito transmission in the People’s Republic of China.

Imported case: a malaria case or infection in which the infection was acquired outside the area in which it was diagnosed. Here, it refers to the patient who acquired the illness from a known malaria-prevalent region outside the People’s Republic of China.

Induced case: a case in which the origin of the illness can be traced to a blood transfusion or other form of parenteral inoculation of the parasite but not to transmission by a natural mosquito-borne inoculation.

Introduced case: a case contracted locally with strong epidemiological evidence linking it directly to a known imported case (first-generation local transmission).

Relapse case: a malaria case attributed to activation of hypnozoites of P. vivax or P. ovale acquired previously.

Recrudescent case: recurrence of asexual parasitaemia of the same genotype(s) that caused the original illness due to incomplete clearance of asexual parasites after antimalarial treatment.

Clinically diagnosed case: an individual with malaria-related symptoms (fever [axillary temperature ≥37.5 °C], chills, severe malaise, headache, or vomiting) at the time of examination.

Laboratory-diagnosed case: a clinical case confirmed by microscopy, polymerase chain reaction, or rapid diagnostic tests in the laboratory.

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