Malaria eradication within a generation: ambitious, achievable, and necessary

Malaria was once one of the most serious public health problems in China. However, the disease burden has sharply declined and epidemic areas have shrunk after the implementation of an integrated malaria control and elimination strategy, especially since 2000. In this review, the lessons were distilled from the Chinese national malaria elimination programme and further efforts to mitigate the challenges of malaria resurgence are being discussed. A retrospective evaluation was performed to assess the changes in malaria epidemic patterns from 1950 to 2017 at national level. The malaria data before 2004 were collected from paper-based annual reports. After 2004, each of the different cases from the Infectious Diseases Information Reporting Management System (IDIRMS) was closely examined and scrutinized. An additional documenting system, the National Information Management System for Malaria, established in 2012 to document the interventions of three parasitic diseases, was also examined to complete the missing data from IDIRMS. From 1950 to 2017, the occurrence of indigenous malaria has been steeply reduced, and malaria-epidemic regions have substantially shrunk, especially after the launch of the national malaria elimination programme. There were approximately 30 million malaria cases annually before 1949 with a mortality rate of 1%. A total of 5999 indigenous cases were documented from 2010 to 2016, with a drastic reduction of 99% over the 6 years (2010, n = 4262; 2016, n = 3). There were indigenous cases reported in 303 counties from 18 provinces in 2010, but only 3 indigenous cases were reported in 2 provinces nationwide in 2016. While in 2017, for the first time, zero indigenous case was reported in China, and only 7 of imported cases were in individuals who died of Plasmodium falciparum infection. Malaria elimination in China is a country-led and country-owned endeavour. The country-own efforts were a clear national elimination strategy, supported by two systems, namely a case-based surveillance and response system and reference laboratory system. The country-led efforts were regional and inter-sectoral collaboration as well as sustained monitoring and evaluation. However, there are still some challenges, such as the maintenance of non-transmission status, the implementation of a qualified verification and assessment system, and the management of imported cases in border areas, through regional cooperation. The findings from this review can probably help improving malaria surveillance systems in China, but also in other elimination countries.

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Ready for malaria elimination: zero indigenous case reported in the People’s Republic of China

Continuous vector pathogen surveillance is essential for preventing outbreaks of mosquito-borne diseases. Several mosquito species acting as vectors of Japanese encephalitis virus (JEV), dengue virus, Zika virus, malaria parasites and other pathogens are primary mosquito species in Shanghai, China. However, few surveys of human pathogenic arboviruses in mosquitoes in Shanghai have been reported in the last ten years. Therefore, in this study, we evaluated mosquito activity in Shanghai, China during 2016 and tested for the presence of alphaviruses, flaviviruses, orthobunyaviruses and several parasitic pathogens. Five pooled samples were JEV-positive [4/255 pools of Culex tritaeniorhynchus and 1/256 pools of Cx. pipiens (s.l.)] based on analysis of the NS5 gene. Alphaviruses, orthobunyaviruses, Plasmodium and filariasis were not found in this study. Phylogenetic and molecular analyses revealed that the JEV strains belonged to genotype I. Moreover, newly detected Shanghai JEV strains were genetically close to previously isolated Shandong strains responsible for transmission during the 2013 Japanese encephalitis (JE) outbreak in Shandong Province, China but were more distantly related to other Shanghai strains detected in the early 2000s. The E proteins of the newly detected Shanghai JEV strains differed from that in the live attenuated vaccine SA14-14-2-derived strain at six amino residues: E130 (Ile→Val), E222 (Ala→Ser), E327 (Ser→Thr), E366 (Arg→Ser/Pro), E393 (Asn→Ser) and E433 (Val→Ile). However, no differences were observed in key amino acid sites related to antigenicity. Minimum JEV infection rates were 1.01 and 0.65 per 1000 Cx. tritaeniorhynchus and Cx. pipiens (s.l.), respectively. Five new Shanghai JEV genotype I strains, detected after a ten-year hiatus in local mosquito surveillance, were genetically close to strains involved in the 2013 Shandong JE outbreak. Because JEV is still circulating, vaccination in children should be extensively and continuously promoted. Moreover, JEV mosquito surveillance programmes should document the genotype variation, intensity and distribution of circulating viruses for use in the development and implementation of disease prevention and control strategies.

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New strains of Japanese encephalitis virus circulating in Shanghai, China after a ten-year hiatus in local mosquito surveillance.

Novel Approaches to Control Malaria in Forested Areas of Southeast Asia.

Tengchong County was one of the counties located at the China-Myanmar border with high malaria incidence in the previous decades As the pilot county for malaria elimination at the border area, Tengchong County is aiming to be the first county to achieve malaria elimination goal A cross-sectional entomological survey was carried out to evaluate the feasibility of elimination approach and assess the receptivity of malaria reintroduction Light traps associated with live baits were used to investigate the abundance of adult mosquitoes in nine villages in Tengchong County Light traps were set to collect adult mosquitoes in both human houses and cowsheds from dusk till dawn in each site A total of 4948 adult Anopheles mosquitoes were collected from May to December in two villages Of the mosquitoes were captured, 242% were in human houses and 758% in cowsheds The peak of abundance occurred in July for An sinensis and in September-October for An minimus (sl) Ten Anopheles species were collected, the most prevalent being An sinensis (503%), An peditaeniatus (316%) and An minimus (sl) (158%), contributing to 976% of the sample Potential breeding sites were also investigated and a total of 407 larvae were collected, with An sinensis (501%) and An minimus (sl) (462%) as predominant species Ponds and rice fields were the two preferred breeding sites for Anopheles mosquitoes; however, the difference between the number of adults and larvae captured suggest other breeding sites might exist Both An sinensis and An minimus (sl) were found zoophilic with human blood index as 021 and 026, respectively No Plasmodium positive Anopheles specimens were found by PCR among 4,000 trapped mosquitoes Although no indigenous malaria cases have been reported in Tengchong County since 2013, there is still a risk from the presence of vectors in the context of human population movements from neighboring malaria endemic areas The presence of An sinensis, associated to rice fields, is particularly worrying Sustained entomological surveillance is strongly suggested even after malaria elimination certification

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Monitoring of malaria vectors at the China-Myanmar border while approaching malaria elimination

The re-establishment of malaria has become an important public health issue in and out of China, and receptivity to this disease is key to its re-emergence. Yingjiang is one of the few counties with locally acquired malaria cases in the China–Myanmar border in China. This study aimed to understand receptivity to malaria in Yingjiang County, China, from June to October 2016. Light-traps were employed to capture the mosquitoes in 17 villages in eight towns which were categorized into four elevation levels: level 1, 0–599 m; level 2, 600–1199 m; level 3, 1200–1799 m; and level 4, > 1800 m. Species richness, diversity, dominance and evenness were used to picture the community structure. Similarity in species composition was compared between different elevation levels. Data of seasonal abundance of mosquitoes, human biting rate, density of light-trap-captured adult mosquitoes and larvae, parous rate, and height distribution (density) of Anopheles minimus and Anopheles sinensis were collected in two towns (Na Bang and Ping Yuan) each month from June to October, 2016. Over the study period, 10,053 Anopheles mosquitoes were collected from the eight towns, and 15 Anopheles species were identified, the most-common of which were An. sinensis (75.4%), Anopheles kunmingensis (15.6%), and An. minimus (3.5%). Anopheles minimus was the major malaria vector in low-elevation areas (< 600 m, i.e., Na Bang town), and An. sinensis in medium-elevation areas (600–1200 m, i.e., Ping Yuan town). In Na Bang, the peak human-biting rate of An. minimus at the inner and outer sites of the village occurred in June and August 2016, with 5/bait/night and 15/bait/night, respectively. In Ping Yuan, the peak human-biting rate of An. sinensis was in August, with 9/bait/night at the inner site and 21/bait/night at the outer site. The two towns exhibited seasonal abundance with high density of the two adult vectors: The peak density of An. minimus was in June and that of An. sinensis was in August. Meanwhile, the peak larval density of An. minimus was in July, but that of An. sinensis decreased during the investigation season; the slightly acidic water suited the growth of these vectors. The parous rates of An. sinensis and An. minimus were 90.46 and 93.33%, respectively. The Anopheles community was spread across different elevation levels. Its structure was complex and stable during the entire epidemic season in low-elevation areas at the border. The high human-biting rates, adult and larval densities, and parous rates of the two Anopheles vectors reveal an exceedingly high receptivity to malaria in the China–Myanmar border in Yingjiang County.

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Receptivity to malaria in the China-Myanmar border in Yingjiang County, Yunnan Province, China.

China has initiated the National Malaria Elimination Action Plan, which aims to eliminate malaria by 2020. However, the transmission of malaria occurs sporadically or in distinct foci, which greatly hampers progress toward elimination in China and other countries. The object of this study was to foci categorization and evaluates whether the response met the requirements issued by the nation or WHO. Residual transmissions were investigated and located with fine spatial resolution mapping from parasitological confirmed malaria cases by use of routine national surveillance data. The “1–3-7” timeframes were monitored for each focus between 2012 and 2015. Each focus was identified, and the application of appropriate measures was evaluated. A total of 5996 indigenous cases were recorded between 2010 and 2015; during this period, the number of cases declined by 99.1% (2010, n = 4262; 2015, n = 39). Most indigenous cases (92.5%) were reported in Anhui (n = 2326), Yunnan (n = 1373), Henan (n = 930), Hubei (n = 459), and Guizhou (n = 458). The temporal distribution showed that the indigenous malaria cases were clustered during the period of May to August. A total of 320 foci were carefully investigated and analyzed: 24 were active foci; 72, residual non-active foci; and 224 cleared-up foci. For the foci response evaluation, all the active foci were investigated within 7 days, while 80.2% of the residual non-active foci were responded within 7 days. In addition, reactive case detection (RACD) was carried out with 92.9% of the active foci and vector investigation carried out with 75%. For residual non-active foci, RACD was carried out with 83.2% and vector investigation with 78.2% of the foci. This study used nationwide data to categorize foci in China and evaluate the response of these areas during the control and elimination phases. Our approach stratifies future control responses by identifying those locations where the elimination of endemic transmission is needed, such as in the counties at the China–Myanmar border and in Tibet. In addition, this study will help local CDC staff to reassess their needs and responses against different types of foci during the elimination and post-elimination phases.

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Mapping transmission foci to eliminate malaria in the People’s Republic of China, 2010–2015: a retrospective analysis

Malaria cases have dramatically declined in China along the Myanmar border, attributed mainly to adoption of the 1-3-7 surveillance and response approach. No indigenous cases have been reported in China since 2017. Counties in the middle and southern part of the border area have a higher risk for malaria importation and reestablishment after elimination.

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Epidemiologic Analysis of Efforts to Achieve and Sustain Malaria Elimination along the China-Myanmar Border.

Vector control is an important approach to preventing and controlling malaria. From the malaria epidemic to malaria elimination in China, vector control has played an essential and irreplaceable role in the historical process. This review systematically summarizes the evolution, adjustment, and optimization of vector control strategy towards elimination and discusses the challenges ahead.This review first summarizes the evolution of vector control strategies during different stages of malaria epidemic, control, elimination, and post-elimination in China. We then distill the vector control experience and lessons in different stages. We discuss the current and future challenges and propose future research directions and developments for novel malaria vector control strategies.Vector control has played an invaluable role in achieving malaria elimination. China adopted different prevention and control measures in response to the different malaria-endemic situations and vector distributions. Firstly, baseline surveys were initiated to establish the entomological data and helped clarify the prevention priorities and targets. Secondly, targeted and adjusted vector control strategies were conducted in various regions according to the local epidemic characteristics and different vector species. Thirdly, scientific research facilitated efficient vector-control strategies. In addition, the overall economic and social development have promoted environmental improvement, personal protection, and health care. Prediction of the vector distribution was integrated into risk assessment strategies, allowing for sustaining achievements in risk areas.The tailored and adapted vector control strategies have played a critical role in China's malaria prevention, control, and elimination. Achievements and lessons learned on vector control from this progress would provide a practical reference in coping with the challenges and potential barriers other countries face in the global effort to eliminate malaria. 

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Hong Tu

Papers

Ready for malaria elimination: zero indigenous case reported in the People’s Republic of China

Receptivity to malaria in the China-Myanmar border in Yingjiang County, Yunnan Province, China.

Mapping transmission foci to eliminate malaria in the People’s Republic of China, 2010–2015: a retrospective analysis

Epidemiologic Analysis of Efforts to Achieve and Sustain Malaria Elimination along the China-Myanmar Border.

Vector control in China, from malaria endemic to elimination and challenges ahead