Background

Historically, malaria has been one of the most important infectious diseases in China. Hainan and Yunnan provinces were the main malaria transmission areas in the People's Republic of China [6]. In 2002, forest goers (30.9%, 95/307) were more than twice as likely to be infected than non-forest-goer residents (15.2%) [7]. In 1991, an investigation in Nanqiao of Wanning City showed that the infection rate of malaria among forest goers (49.4%, 118/239) was significantly higher than that among non-forest-goers (8%, 11/138) [8]. The factors related to malaria infection rate in forest goers including the frequency of staying in the mountains, whether to take antimalarial chemoprophylaxis, the acceptance of antimalarial propaganda, and mosquito control measures [9–11]. Hainan Island has been engaged in malaria control and elimination in forest goers since the 1990s. Been supported by the Global Fund to Fight AIDS, Tuberculosis and Malaria, the strategy for the prevention and control of malaria in forest goers  including mass drug administration (MDA) that focused on patients and the surrounding population (family members or co-workers), epidemiology investigations on patients, timely surveillance of vector dynamics, and vector control measures [such as insecticide residual spraying (IRS), insecticide-treated nets (ITNs) or long-lasting insecticidal nets (LLINs)], has been intensified since 2003 [12]. Seasonal anti-malaria measures were carried out uninterruptedly in spring and autumn annually in Hainan resulting in a decline of malaria incidence [13].

In 2010, Hainan joined the National Malaria Elimination Programme (NMEP). In Hainan Island there were eight Class I counties (endemic counties of P. falciparum) and ten Class II counties (endemic counties of P. vivax) [14]. Hainan Island officially launched malaria elimination in 2011. Subsequently, the 1-3-7 approach have been applied in the disposal of foci since 2012, which refer as following: case reporting within 1 day, case investigation within 3 days, and focus investigation and action within 7 days. Under the requirement of 1-3-7 approach, every reported case was confirmed by microscopy and PCR, and every focus file was collected and reported through the Parasitic Diseases Information Reporting Management System (PDIRMS). The last indigenous malaria case of P. vivax in Hainan was reported in Sanya in 2012.

From 2013, only imported malaria cases were reported in Hainan Island, and every imported malaria focus was classified and disposed according to the guidelines of the 1-3-7 approach. In 2015, there was an outbreak reported in Sanya, which was induced by indigenous cases infected by P. malariae among forest goers [15]. Based on the 1-3-7 approach, an innovative three-layer strategy (TLS) was designed and applied in the disposal of outbreak in 2015. From 2016 to 2018, the effectiveness of TLS was evaluated and mass drug administration by chemoprophylaxis were conducted in three layers. Hainan Province has achieved the goal of elimination malaria in 2019 and acquired the WHO certification of malaria elimination by field in 2021 [16]. This article summarizes the prevention and control measures of TLS strategy which administrated during the P. malariae malaria outbreak in 2015, and further outlines the lessons learned from the generation to evaluation from process.

An outbreak of P. malariae malaria occurred in Sanya City, Hainan in 2015

The first malaria case was reported on September 7, 2015. A total of six indigenous P. malariae cases were sequentially detected by ACD and PCD surveillance. All of them were male farmers aged from 19 to 40 years. This outbreak was reported from three villages (Baolong, Zhanan, Lixin) of Gaofeng town in Sanya City, respectively. Four cases in September, one case each in October and November, and no more cases were detected by PCD after that (Fig. 1).

Fig. 1
figure 1

Information on the schedule of case exposure time and frequency, the method of detection, diagnosis and epidemiological characteristics in this outbreak. ACD active case detection, PCD passive case detection, CDC Center for Diseases Control and Prevention

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Case 1 Male, 31 years, farmer, lived in Baolong village. On September 7, 2015, a male outpatient with chills, fever, headache, and limb weakness was diagnosed with P. malariae infection by blood smear microscopy in Sanya Hospital of Agricultural Reclamation (SYAR). The case subsequently confirmed by blood smear microscopy and PCR in Hainan Provincial Malaria Diagnosis Lab (HPMDL). Combined with the epidemiological history (without overnight in abroad and blood transfusion) and laboratory findings, he was determined as an indigenous case, and further classified as forest goer (Case 1). According to the information provided by Case 1, another three co-workers were confirmed as the new cases by blood smear microscopy and PCR (Case 2: Male, 19 years, farmer, lived in Lixin village; Case 3: Male, 27 years, farmer, lived in Lixin village; Case 4: Male, 31 years, farmer, lived in Lixin village). The four cases reported to stay overnight to collect bodhi fruit.

Case 5 Male, 40 years, farmer, lived in Zhanan village. On October 17, 2015, a male outpatient with chills, fever, headache, and limb weakness was diagnosed with P. malariae infection by blood smear microscopy in Nandao Township Hospital. The case subsequently confirmed by blood smear microscopy and PCR in HPMDL. Considering the epidemiological history (without overnight in abroad and blood transfusion) and laboratory findings, he was also determined as an indigenous case and classified as a forest goer.

Case 6 Male, 25 years, farmer, lived in Lixin village. On November 26, 2015, a symptomatic malaria carrier was found by PCR in HPMDL after TLS implemented. Subsequently, the case was confirmed by microscopy as P. malariae infection. However, Case 6 had no history of overnight slee** in mountain, and classified as a victim in village.

All cases were sequentially transferred to SYAR and hospitalized to receive treatment with a standard regimen of oral chloroquine phosphate for 3 days (600 mg on 1st day, and then 300 mg once a day on the 2nd and 3rd days of therapy), plus primaquine diphosphate for 8 days (22.5 mg per day) to ensure therapeutic compliance.

Design of TLS and its application in the 2015 outbreak

Based on the geographical distribution of five malaria cases (Case 1, 5 by PCD, and Case 2, 3, 4 by ACD), history of malaria joint defence and work urgency of elimination malaria, an innovative three-layer strategy (TLS, Fig. 2) was designed for expanded screening, PCD and ACD were optimally conducted as described in a previous study [17–19]. TLS was applied to prevent malaria transmission in the 2015 outbreak, more details showed as below, and the scope of three layers in details have showed in Additional files 1 and 3.

Fig. 2
figure 2

The skeleton map of three-layer strategy applied from 2015 to 2018 in Hainan. The red frame represents applied in the first layer only, but the blue frame represents various measures depend on different layers. IRS indoor residual spraying, TLS three-layer strategy, LLINs long lasting insecticide nets, JPCS joint prevention and control strategies, ACD active case detection, PCD passive case detection, MPD malaria parasite detection, VS vector surveillance, ACT attendees of capacity training, MC mass chemoprophylaxis

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First layer

The villages with five malaria cases (Baolong, Zhanan and Lixin in Gaofeng Town, Sanya City) and adjacent villages, were regarded as the first layer. All residents who lived in the first layer were considered as the high-risk population (HRP). ACD screening was taken as primary measure in all residents by blood smear microscopy and SSU rRNA PCR assay [20], and PCD acted as complementary measure. During the implementation of  ACD, a total of 1774 slides were screened by blood smear microscopy and PCR. Thirteen positive samples were found by PCR. Confirmed by experienced microscopists from HPMDL, only Case 6 were identified and determined as indigenous cases of P. malariae infection (Table 1).

Second layer

The Gaofeng Town and ten adjacent towns, which involved to Yucai in Sanya city, Daan and Zhizhong in Ledong County, ** tourism resources for economic development [34], where the challenges in the control and prevention of imported malaria, forest goers remain as a high-risk group.

TLS was firstly applied in the 2015 outbreak, but there was no more similar scenarios in China can be used to explore scopes of the TLS for practicability after 2015. In addition, although there were at least two transmission chains in the perspective of epidemiological investigation, the relationship between two transmission chains is not certain and further investigation is urgently need.

Conclusions

The innovative TLS was effective in blocking the outbreak by P. malariae among forest goers in Hainan at malaria elimination stage. However, it still need to be tailored to apply in malaria control or elimination in similar settings for outbreak disposal. Moreover, whether it could prevent re-establishment by the potential malaria in the post-elimination phase needs to be further assessed.