Changing Landscape of Malaria in China

Abstract

Large-scale malaria control activities in China have been conducted with significant success, since the launch of the nationwide malaria control program. This study investigated the malaria distribution in China, particularly in provinces with high risks. Spatial and temporal data were assembled for all endemic or historically endemic areas and combined to identify common patterns and to investigate the actual changes in the burden of malaria in the country. Data were analyzed and the progress in malaria elimination feasibility was discussed. The results indicated that the current distribution of malaria and vectors associated could provide evidence on the assessment of the feasibility of the malaria elimination in China.

Keywords

malaria control malaria elimination malaria in China

Introduction

Malaria is, and has been, the most important parasitic disease of man in terms of mortality, morbidity^1-3 and effect on life generally, using “parasitic” in the narrower meaning of the animal parasites: worms and protozoa.⁴

Historically, malaria has been a major health problem in China and references to what was almost certainly malaria occur in Chinese document from about 2700 bc.⁵ The ancient Chinese medical writings (The Nei Ching) from 4700 years ago apparently refers to paroxysmal fevers associated with enlarged spleens and a tendency to epidemic occurrence.⁶ In the 1920s and 1930s, antimalarial efforts started to involve epidemiologic studies.⁷ Prior to 1949, approximately 30 million malaria cases occurred in the country each year, with some localities having parasite incidence rates as high as 800 cases per 1000 population.⁷ Large-scale malaria control activities have been conducted with significant success since the launch of the nationwide malaria control program in 1955. As elsewhere, the emphasis during these early campaigns was on insecticide household spraying.^8-10 Together with the building of a preventive and anti-epidemic infrastructure and health care system as well as the training of personnel, the government used techniques of mass mobilization to launch programs of vector control and mass therapy. Provinces were also organized into antimalarial regional alliances to facilitate malaria control and surveillance.⁷ There was evidence for the efficacy of malaria control interventions,¹¹ their cost-effectiveness,¹² and a significant increase in funding for malaria control nationwide.

Recent studies have examined malarial distribution patterns around the world, including the global distribution of malaria,¹³ population at risk,¹³ and the global distribution of falciparum malaria.^1,14 Others studies have investigated malaria distribution patterns in China, particularly in provinces with high malaria risks. For instance, studies have examined the geographic distributions, demographic patterns, and temporal trends of falciparum malaria in China,⁹ spatial distribution and clustering of malaria in Anhui,¹⁵ and spatiotemporal distribution pattern of malaria in Yunnan¹⁶ and in Hainan.^17,18 In this study, we aim to identify common patterns and investigate the actual changes in the burden of malaria in China. We undertake case studies of several provinces to explore the central trends, using available data from similar or related published scientific studies.

Methods

Assuming that the most common channel of communication in the scientific community for sharing information about emerging and endemic diseases is publication in scientific journals, we performed a comprehensive literature review of notified malaria cases using retrospective study. An electronic data search was undertaken through Medline to identify a complete review from World Health Organization, UNICEF, Roll Back Malaria, the World Bank, National Program for Malaria Control, and other scientific reports. Criteria for selection included all reported scientific publications related on malaria morbidity and mortality risks, defined through epidemiological studies. Selected studies regions were classified, as high malaria endemic, with potential malaria transmission or historically or currently malaria free. All articles were reviewed to identify the studies meeting the criteria for selection. We included reports of laboratory that confirmed Plasmodium for both endemic and epidemic events. Full articles were obtained for all original reports. To identify articles for reported malaria events, we used different keywords: malaria burden, malaria control in China, cost-effectiveness, vector control, malaria transmission, malaria epidemic, malaria endemic, insecticide-treated nets (ITNs), indoor residual spraying (IRS), and artemisinin-based combination therapy. We identified regions where malaria is endemic or has been endemic in the past. Then, we compared the temporal and geographical distribution of cases reported. The classification of a region as malaria endemic is not necessarily based on malaria cases and deaths reported in the regions health information system or in general literature. Some provinces where great effort has been made for reducing malaria burden were considered among the malaria endemic. This was done because in remote areas; particularly at the village level, many people are treated at home or in private facilities that do not report to the national health information system. We consider that a region is malaria free when it meet the criteria of a malaria-free area (zero incidence over 3 consecutive years) as defined by the World Health Organization. We also use sibling history data from household surveys and published works reporting population-based studies of insecticide coverage for both national and subnational.

Results

This study shows that great efforts to control malaria in China have been made over the past 50 years, resulting in a significant and continued decline of the prevalence between 1984 and 1993; however, the incidence rate has risen slightly since 2001 with occurrence of local outbreaks in some regions where the disease had previously disappeared. The annual incidence rates of malaria were 3.07, 4.62, 3.57, and 3.38 per 100 000 from 2005 to 2008, respectively. We noticed that the epidemiology of malaria in China is strongly linked to geographical situation and the characteristics of the region (Table 1). The prevalence of malaria gradually increases from the north to the south. Ecological, demographical, and climatic changes influence the distribution of malaria vectors and consequently have an impact on malaria transmission and the predominant species. In the north of China, malaria was of low endemicity and Plasmodium vivax was the only species present; temporary epidemics were occasionally caused by imported falciparum malaria. The southern part of China used to be the hyper- and meso-endemic regions where falciparum malaria was widely present. In some meso- and hypo-endemic areas, (central China), vivax malaria was predominant, though falciparum malaria also existed and focal outbreaks often occurred. The epidemic situation in China is largely affected by that in the nearby Southeast countries (Table 1 and Figure 1). Yunnan and Hainan provinces still face a severe situation of endemic malaria because of the spread of Plamodium falciparum and imported cases of malaria in 25 border counties in Yunnan province (Figure 1A). According to the data from the National Malaria Survey in 2006, the number of fatal malaria cases in Yunnan province was 32, the highest rate in China, and it accounted for 84.2% of total fatal malaria cases; subtertian malaria imported from abroad accounted for 60.4% of these cases. More than 15 000 cases of confirmed and clinically diagnosed malaria were reported in China in 2008-2009. The majority of cases were from the provinces of Anhui, Yunnan, Henan, Hainan, Jiangsu, and Hubei. However, the absolute number of malaria cases and deaths were estimated as being somewhat higher, as it is difficult for the public health system to detect patients in remotes mountainous areas (Tables 2 and 3). Based on the country’s current malaria situation, all counties are classified as high malaria incidence, with potential for malaria transmission, or historically and currently malaria free. This is intended to the development of priorities for national malaria control strategies by the authorities at national and local level (Table 4).

Table 1.

Characteristics of Malaria Transmission Patterns by Geographical Region.^a

Geographical Region	Type of Malaria	Malaria Inoculation Rate	Immunity of the Population	Transmission Characteristics
North China	Malaria free or very low level	Absent	Absent	Very rare cases; transmission by Plasmodium vivax; sometimes imported cases
Central China	Unstable malaria	Irregular, low to very low	Unreliable in older age groups, absent in those younger than 5 years	Seasonal, irregular contact between vectors and human; transmission by P vivax
South China	Stable, epidemic malaria	Rising suddenly, medium to low	Low or absent; rapidly lost	Variable, subject to rapid and sudden changes; transmission by both P vivax and P falciparum

Table 1 is derived from a collation of information from multiple reports of World Health Organization, National malaria control programs, and reports of scientific publications. Geographical regions limits are defined by their latitude. We considered north China as located above the latitude 33° north, central China as limited between the latitudes 25° and 33° north, and south China as regions below the latitude 25°.

Figure 1.

Malaria morbidity and mortality by endemicity areas in China 2001 and 2003. Spatial distribution of Plasmodium falciparum malaria endemicity in China and borders countries, 2007 endemicity map.

Table 2.

Malaria Morbidity and Mortality by Selected Provinces in China, 2008-2009.^a

Province	Estimated Population	No. of Confirmed Malaria Cases	No. of Malaria Deaths	Percentage of Plasmodium falciparum Among Confirmed Cases	Incidence per 1000	Mortality Rate per 100 000
Anhui	79 185 346	8561	0	0	0.109	0.000
Yunnan	55 573 403	3935	6	25	0.071	0.011
Hainan	10 151 725	688	0	3	0.068	0.000
Hubei	72 868 305	191	1	9	0.003	0.001
Guangxi	61 501 384	43	2	16	0.001	0.003
Shandong	110 823 798	115	5	24	0.001	0.005
Sichuan	100 334 999	96	3	24	0.001	0.003
Henan	108 660 133	1444	2	1	0.012	0.002
Guizhou	59 676 774	243	1	2	0.004	0.002
Jiangsu	87 939 949	469	0	11	0.005	0.000
Zhejiang	55 644 422	459	2	6	0.008	0.004

Source: World Health Organization Western Pacific Region, reports 2008.

Table 3.

Malaria Morbidity and Mortality in China, 2001-2009.^a

Malaria Cases	2001	2002	2003	2004	2005	2006	2007	2008	2009
Reported cases	26 945	172 200	169 828	145 676	100 106	116 260	133 699	135 467	14 491
Confirmed cases	21 237	25 520	28 491	27 197	21 936	35 383	29 304	16 650	9287
Imported cases	—	556	621	1714	2632	2097	1192	780	—
Reported deaths	28	42	52	31	48	38	18	23	—

Source: World Health Organization annual reports and National Malaria Control Program reports 2001-2009.

Table 4.

Priority for Malaria Control Strategies and Classification, by Epidemiological Setting.^a

Epidemiological Setting	Type of Malaria	Control Strategies
Stable endemic and epidemic prone malaria	High malaria incidence	Integrated malaria control program
		Active cases detection and treatment
		Parasitological surveillance, including systematic blood test
		Vectors control by indoor spraying with residual insecticides (IRS) and insecticide-treated bed nets (ITN)
Unstable malaria	Low malaria incidence or with potential malaria transmission	Early and effective cases management including presumptive treatment for suspected cases
		Malaria surveillance programs and home management where appropriate
		Clinical confirmation for suspected cases
Malaria free	Historically or currently malaria free	Prevention of imported malaria cases for travelers from malarial areas
		Early and effective cases management in suspected cases
		Diagnosis for clinical confirmation and treatment

Data from a collation of information from multiple scientific publications.

Discussion

Malaria was historically an endemic disease China,¹⁹ with prevalence varying from very high to low. The results reported here come from a strong national level monitoring and evaluation system developed through the National Malaria Control Program. We analyzed past and recent data from standardized national and regional surveys and explored factors associated with the geographical distribution of malaria around China.

In historical times, and as recently as the early to mid-20th century in southern Asia, continual malaria infection and reinfection had devastating effects on the mental, physical, social, and economic conditions of the individuals and communities affected.²⁰ This particular situation has galvanized the national government to establish programs for definitive eradication of the disease, under the broad direction and encouragement of the World Health Organization.²¹ In the second half of the 20th century, China followed its own path. The emergence of strong national government and the absence of major warfare must have contributed significantly to the reductions of its malaria burden in the decades that followed the end of World War II. However, political turmoil within China in the late 1960s and early 1970s prevented major advances. Then, in the mid-1970s, a determined antimalaria campaign was initiated in which vector control was integrated with rigorous malaria case detection and treatment.⁷ Malaria-related deaths in China may now be fewer than several hundred per year, compared with the hundreds of thousands that were sustained through the early decades of the century. The Chinese antimalaria campaign yielded another outstanding contribution. This was the development of the artemisinin derivatives of Quinhaosu, a traditional Chinese herbal medicine, to combat chloroquine-resistant P falciparum. A study has revealed that, in Vietnam, in Southeast Asia, in the early 1990s, artemisinin derivatives contributed dramatically to the reversal of a renewed rise in malaria mortality rates in the region.²² Today these compounds are at the heart of attempts to reformulate global malarial drug policy based on drug combinations that include artemisinin derivatives as a means of combating the emergence and spread of antimalarial drug resistance.^23,24

The incidence of malaria decreased dramatically during the 20th century in China. The epidemiology of the disease is extremely variable, and different situations require different malaria control strategies, adapted to risk groups, vector behaviors, local health infrastructure, and environmental conditions. Studies reveal that climatic conditions have been major factors influencing the distribution of malaria in Asia.²⁵ However, there is evidence of a reemergence of malaria since 2000, with more than 740 000 cases being notified in 2004.²⁶ A thorough examination of the situation and the data provided in the general literature reveals a real gap. There is uncertainty in the data provided, and the real burden of malaria in China is still unknown even though great efforts have been made. The actual number of reported cases is much higher than the reported cases.²⁷ One of the factors responsible for the reintroduction of malaria is a failure of malaria vigilance. The malaria early warning system is not well established in remote and mountainous areas, and the rapid response capability to malaria outbreak by local organizations is limited when cases occur in remote areas.²⁸ Another growing problem in the malaria control system in China, as in the Greater Mekong subregion, has been the proliferation of counterfeit antimalarial drugs on the market. In 2006-2007, an international multidisciplinary group consisting of World Health Organization officials, physicians, pharmacists, scientists, and Interpol officers conducted a joint investigation on counterfeit artesunate in the Mekong countries. From a sample of 391 artesunate collected between 1999 and May 2006 in Vietnam, Cambodia, Lao PDR, Myanmar, and the Thai–Myanmar border, a wide variety of fake artesunate was identified. Studies on the pharmaceutical ingredients in the counterfeits suggested that the manufacturing sites were based in China.²⁹

Conclusion

Substantial progress to reduce the morbidity and mortality cause by malaria in China has been made and encouraged by the National Malaria Control Program. However, elimination of malaria would be feasible if the technical and operational challenge to the permanent interruption of transmission could be overcome. A sufficiently high coverage of malaria intervention to interrupt local transmission and parasite transfer from malaria endemic to nonendemic areas is needed to assess the probability of malaria being reestablished.

Footnotes

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

References

Snow

Guerra

Noor

Myint

Hay

. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005;434:214-217.

Guinovart

Navia

Tanner

Alonso

. Malaria: burden of disease. Curr Mol Med. 2006;6: 137-140.

Centers for Disease Control and Prevention. The impact of malaria, a leading cause of death worldwide. http://www.odc.gov/malaria/impact/index.html. Accessed August 3, 2007.

Bradley

. Malaria: old infections, changing epidemiology. Health Transit Rev. 1992;2(suppl):137-152

Cox

. History of the discovery of the malaria parasites and their vectors. Parasit Vectors, 2010;3:5.

Hoeppli

Parasites and Parasitic Infections in Early Medicine and Science. Singapore: University of Malaya Press; 1959.

Yip

. Antimalarial work in China: a historical perspective. Parasitologia. 1998;40:29-38.

Tang

. Progress in malaria control in China. Chin Med J. 2000;113:89-92.

Lin

Tian

. Spatial and temporal distribution of falciparum malaria in China. Malar J. 2009; 8:130. doi:10.1186/1475-2875-8-130.

10.

Zhou

Wang

Tang

. Malaria situation in the People’s Republic of China in 2005. Chin J Parasit Dis. 2006;24:401-403.

11.

Lengler

. Insecticide-treated bed nets and curtains for preventing malaria. Cochrane Database Syst Rev. 2004;(2):CD000363. doi:10.1002/14651858.CD000363.pub2.

12.

Sabot

Cohen

Hsiang

. Malaria elimination 4. Costs and financial feasibility of malaria elimination. Lancet. 2010;376:1604-1615.

13.

Hay

Guerra

Tatem

Noor

Snow

. The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis. 2004;4:327-336.

14.

Hay

Guerra

Gething

. A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 2009;6:286-302.

15.

Zhang

Wang

Fang

. Spatial analysis of malaria in Anhui province, China. Malar J. 2008;7:206.

16.

Hui

Chen

. Spatio-temporal distribution of malaria in Yunnan province, China. Am J Trop Med Hyg. 2009;81:503-509.

17.

Zhang

Wang

. Study on the distribution of malaria in Hainan province through spatial local interpolation technique [in Chinese]. Zhong Hua Liu Xing Bing Xue Za Zhi. 2003;24:269-271.

18.

Xiao

Long

Wang

. Spatiotemporal distribution of malaria and the association between its epidemic and climate factors in Hainan, China. Malar J. 2010;9:185.

19.

Goh

Phua

. Of men and mosquitos: the story of malaria. Asia Pac J Public Health. 1987;1:95-101.

20.

Carter

Mendis

. Evolutionary and historical aspects of the burden of malaria. Clin Microbiol Rev. 2002;15:564-594.

21.

Expert Committee on Malaria. Report of the second session. Malarial control survey and recommendations. Bull World Health Organ. 1948;(1):213-252.

22.

Schuftan

A Story to Be Shared: The Fight Against Malaria in Vietnam. Hanoi, Vietnam: World Health Organization, Western Pacific Regional Office; 2000.

23.

World Health Organization. The Use of Antimalarial Drugs. Report of a WHO informal consultation (WHO/CDS/RBM/2001.33). Geneva, Switzerland: World Health Organization; 2000.

24.

Zhang

Hiller

. Climate change and the transmission of vector-borne diseases: a review. Asia Pac J Public Health. 2008;20:64-76.

25.

World Health Organization. Antimalarial Drug Combination Therapy. Report of a WHO technical consultation (WHO/CDS/RBM/2001.35). Geneva, Switzerland: World Health Organization.

26.

Chinese Ministry of Health. National Infectious Disease Report. Beijing, China: Ministry of Health; 2004.

27.

Zhong

. Current Status of Malaria in China. Beijing, China: National Institute of Parasitic Diseases, China CDC.

28.

Control of Malaria in East Asia. Report of the Bio-Regional Meeting Shanghai, People’s Republic of China; November 29, 2004.

29.

World Health Organization. Malaria in the Greater Mekong Subregion: Regional and Country Profiles. Geneva, Switzerland: World Health Organization; 2010.