Malaria elimination in the international border areas is one of the challenges that countries face today in their path to malaria elimination. Interruption of malaria transmission and continuous maintenance of malaria free in the Yunnan border area allowed the WHO’s certification of malaria elimination for China [2, 7]. This case study presented the story of malaria from hyperendemicity to elimination in the Yunnan border area. The following experiences and lessons can be learned from this case study.

Experiences

Universal coverage of malaria surveillance

The WHO certification of malaria elimination requires applicant countries to provide evidence that (1) local malaria transmission has been fully interrupted, resulting in zero indigenous human malaria cases for at least the past 3 consecutive years (36 months), and (2) an adequate program for preventing reintroduction of malaria transmission is fully functional throughout the country [17, 28]. The “1-3-7” approach of malaria elimination [24] can only be performed after malaria cases are detected. Finding malaria cases in time is the prerequisite of using the “1-3-7” approach to interrupt and prevent further transmission. To ensure the sensitivity of malaria surveillance, a surveillance system of malaria cases in the border area has gradually achieved universal coverage in the elimination stage, which includes proactive and passive case detection, community-based malaria detection and screening of migrants and travellers in frontier townships. Due to few malaria cases during the elimination stage, malaria diagnosis and treatment can no longer be a money-making channel. Based on the local governmental health policy, private sector, village leaders and village health workers help to monitor migrants and refer febrile patients to perform tests for malaria in health institutions with laboratory test. Remote villages have trained health or malaria workers who can use RDTs to test febrile patients for malaria [10].

Accurate and dynamically adjusted stratification

The WHO recommends that stratification should be initially performed at the lowest geographical level for which operational decisions can be made [17]. In the 1990s, Yunnan developed natural village-based stratification to perform cost-effective interventions, and the stratification and intervention measures were adjusted every year [19]. Appropriate investment made it possible to fully carry out natural village-based stratification and interventions from 2003 to 2013. The integrated interventions dramatically reduced the malaria burden. The WHO also recommends that interventions are expected to change the epidemiology of malaria rapidly and profoundly, and the stratification of malaria maps should be revised frequently. As transmission intensity is progressively reduced, stratification needs to include vulnerability and receptivity to malaria [17].

“The Action Plan of China Malaria Elimination (2010–2020)” defined a county as a unit of elimination. The 25 border counties were categorized into two tiers according to the national stratification standards for malaria elimination, namely 17 type I counties and eight type II counties [25, 26]. Yunnan interrupted malaria transmission in 2017, and the national stratification standards for malaria elimination were no longer suitable for the actual situation. Yunnan stratified the 25 border counties into three types (A, B and C) in 2017 and then identified 16 natural villages with high risks of border-spill malaria in 2018 (Additional file 1) to guide resource allocation and the use of a more targeted strategy.

Based on the experiences of malaria control from hyperendemicity to elimination, Yunnan designed the “3 + 1” strategy in 2019 to prevent reintroduction of malaria transmission, namely, (1) comprehensive and intensive malaria interventions in the area within a 2.5 km wide perimeter along the international border to prevent border-spill malaria, (2) community-based malaria surveillance to identify international migrants with possible malaria in the frontier townships, (3) consolidate surveillance into normal health services to maintain vigilance of health personnel to malaria signs, and + 1) emphasize the need to strengthen collaboration with neighboring countries to reduce their malaria burden with a clear focus on border areas with China [10]. The “3 + 1” strategy is in accordance with the principle of the WHO recommended malaria elimination strategy [17].

Clearing parasite reservoirs

A comprehensive malaria control strategy includes clearing parasites with antimalarial treatments, interrupting transmission by vector control and protecting vulnerable individuals. Drug-based treatment is the primary intervention in malaria control and elimination, and clearing parasites with antimalarial drugs is the most direct and effective approach. Asymptomatic and submicroscopic parasite density, especially for P. vivax, and limitations of microscopist ability and RDTs may lead to underdetection or misdiagnosis [18, 22]. To clear parasite reservoirs for the reduction of malaria infectious sources, expanded clinical and radical cure treatments were conducted in highly endemic years in the border area. The expanded clinical treatment is that the treatment includes both lab confirmed cases and suspected malaria cases in health facilities. The expanded radical cure treatment is that treatment includes people with both history of lab confirmed malaria and suspected malaria in the last 2 years. The ratios of clinical and radical cure treatment to laboratory-confirmed malaria cases were approximately three during 2003‒2006. To accelerate the malaria elimination process, the ratio of radical cure treatment versus laboratory-confirmed malaria cases reached 17.3 in 2010 due to the expanded radical cure treatment (Table 2). Based on these experiences and results of the intervention trial in Cambodia [32], mass drug administration can rapidly reduce the malaria burden in hyperendemic areas; however, it might not be necessary for mesoendemic situations. When malaria endemicity is still high, treatment for all confirmed, clinical and suspected cases, not just targeting confirmed malaria cases, might be necessary [18, 22]. After parasite reservoirs cleared, clinically presumptive treatment of suspected cases is not recommended again. Confirmatory diagnosis for treatment with antimalarial drugs is recommended and practiced because of a few of malaria cases and the high accessibility of laboratory malaria diagnosis for people in the border area. The high accessibility of laboratory test for malaria is assured by the improvement of the laboratory test capacity in public health facilities and the locally improved transportation for residents.

Comprehensive interventions

A systematic network literature review compared malaria prevention measures, including ITNs including long lasting insecticidal bed nets and insecticidal-treated bed nets, IRS, prophylactic drugs (PD) and untreated nets (UN), against no intervention. The study demonstrated that only ITN [rate ratio (RR): 0.5, 95% CI: 0.3–0.7] showed preventive efficacy precision while other methods, PD (RR: 0.2, 95% CI: 0.004–15.4), IRS (RR: 0.6, 95% CI: 0.2–1.6) and UN (RR: 0.7, 95% CI: 0.3–1.9), indicated considerable uncertainty associated with their point estimates [33]. The results of the review document that no single preventive measures can certainly prevent malaria. An analysis of simulated trial data using a transmission model also documents that a longer duration of prophylaxis leads to a greater measured efficacy of radical cure treatment for P. vivax, particularly at higher transmission intensities [34]. The results of this study indicate that integrated interventions are more effective than a single measure.

To control and eliminate malaria, integrated interventions, including proactive and passive case detection, vector surveillance and evidence-based vector control and preventive treatment with drugs, have been used in the border area. In the border area, approximately 100 thousand people received prophylactic drugs for prevention in 2003, and then approximately 2500 people in border communities that neighbouring with the hyperendemic areas of Myanmar received prophylactic drugs to prevent border-spill malaria in 2020. Because of lacking the powerful data on border-spill malaria caused by anopheline mosquitoes infected with malaria parasites, the WHO just recommends prophylactic drugs for travellers in malaria endemic countries, not in the setting of malaria elimination [17, 28]. There is a viewpoint that prophylactic drugs should no longer be used in the phase of malaria elimination in China. However, when vector control measures cannot effectively prevent border-spill malaria, the intervention of prophylactic drugs is still needed for people residing in communities bordering the hyperendemic areas of neighboring countries [10] as well as travellers who want to go to endemic countries [22].

Lessons

Reduced collaboration increased the risk of malaria reintroduction

Communication and collaborative activities were significantly reduced after China’s GFATM malaria project was terminated in 2014. A slight malaria resurgence has appeared in some border areas of Myanmar since 2014 [18, 35]. The number of imported malaria cases correspondingly increased from 358 in 2013 to 594 cases in 2015 in Yunnan. The Laiza and nearby areas of KR2 with a population of approximately 30 thousand persons, are one of the malaria hotspot areas in the border area of Myanmar [10]. The number of reported malaria cases increased from 518 in 2013 to 2367 in 2016. The strengthened collaborative interventions between China and Myanmar during 2017‒2019 reduced the number of malaria cases to 274 in 2019. However, reduced collaborative interventions due to the COVID-19 pandemic led to malaria resurgence again, and a total of 1532 cases were reported in Laiza and nearby areas of KR2 from January to November 2021. The example of Laiza and nearby areas documents that reduced communication and collaboration may increase malaria incidence in the border areas of neighbouring countries and increase the risk of malaria reintroduction in China. In contrast, a reduction in malaria burden in the border area of neighbouring countries can help decrease the threat of malaria importation and reintroduction.

Maintaining vigilance of health personnel

Vigilance of health personnel, especially clinical doctors in hospitals, is critical to reduce imported malaria death and prevent reintroduction of malaria transmission in elimination settings [17, 28]. Under the current technical and transportation conditions in China, travelers from malaria-endemic countries can always obtain laboratory tests for malaria in time as long as clinical doctors recognize the necessity of test. In fact, a number of imported malaria deaths are mainly attributable to the delayed diagnosis of malaria because of clinical doctors losing their vigilance. For example, in November 2021, a Burmese patient with kidney failure was hospitalized in a county hospital in the border area. His resident doctor did not recognize the necessity of malaria testing for more than 3 weeks because of the lack of vigilance for malaria. The patient had to be moved to a high-level hospital due to his worsened condition, and then the high-level hospital tested him with P. malariae, which was one of the reasons for his kidney failure. Reducing vigilance and technical capacity in malaria diagnosis and treatment due to rarely seeing malaria patients anymore is therefore one of the challenges to prevent the reintroduction of malaria transmission in elimination settings [10].

Challenges in the context of the COVID-19 pandemic

The Yunnan border area is also one of the areas facing a high risk of the COVID-19 pandemic in China. To fight the COVID-19 pandemic, some human and financial resources were moved from malaria control to the response to the COVID-19 pandemic. In July 2021, when Yunnan tried to communicate with the Health Authority of Myanmar KR2 to collaborate in rolling back the resurgence of malaria, the KR2 Department of Health responded that they were too busy responding to the COVID-19 pandemic to have human resources fighting malaria. Although the border crossing is strictly limited under the context of the COVID-19 pandemic in Yunnan, the increased malaria incidence in the KR2 has led to malaria spilling over the boundary by Anopheles mosquitoes into communities in the Yunnan border area. From January to November 2021, Yingjiang County reported a total of 70 cases, and 63 of them were categorized into border-spill malaria cases. In the context of the COVID-19 pandemic and border collaboration limitations for malaria, comprehensive intervention, including proactive and passive case detection, vector surveillance, evidence-based vector control and preventative treatment with antimalarial drugs, should be undertaken to prevent border-spill malaria within a 2.5 km-wide perimeter along the boundary in Yunnan [10].

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