Management of imported malaria cases and healthcare institutions in central China, 2012–2017: application of decision tree analysis

In spite of unprecedented global success in fighting malaria during first decade of the twenty-first century, performance has begun to plateau, chiefly resulting from limited funds, regional conflicts, abnormal climate, resistance of parasites to anti-malarials and resistance of mosquitoes to insecticides [1‐4]. In addition, global economic integration and consequential increase in mobility of populations has not confined malaria to former geographic distribution, making control efforts complicated and progress towards elimination slow down [5‐8].

China is a model of countries progressing to malaria elimination. As China forms close connections with many countries, just like its partners all over the world, malaria is undergoing profound changes. From 2006 to 2016, malaria cases in China decreased from 64,178 to 3142. Under the National Malaria Elimination Action Plan (2010–2020) (NMEAP) by the former Ministry of Health [9], Chinese indigenous cases sharply declined by 99.9% from 4262 cases in 2010 to three cases in 2016. China has entered the post-elimination era of malaria since, for the first time in 2017, there was no indigenous case reported [10]. Conversely, imported malaria cases increased and became a main challenge to malaria elimination in China [11].

Plasmodium falciparum, mainly imported from other countries, has taken the place of Plasmodium vivax that was historically the predominant species in China [10, 12]. Henan Province achieved the goal of zero indigenous malaria cases since 2012, 2 years after the initiation of NMEAP, whereas imported malaria cases, consisting chiefly of P. falciparum, have increased and become the foremost challenge to malaria elimination [13, 14].

Malaria cases in Henan Province after 2012 were mainly introduced from African countries where P. falciparum was the most prevalent malarial species [15]. Labourers infected by malaria parasites returning from African countries to their hometowns, primarily scattered in vast rural areas, bring randomized and sporadic cases to medical personnel unfamiliar with rare malaria cases or with the potential for fatality in cases of falciparum malaria [16]. After 2010, at the start of the NMEAP, the fatality rate from malaria in China increased and more than four-fifths of deaths had severe complications, such as brain lesions, shock, severe liver/kidney lesions, haemolysis [17]. Henan Province ranked first in the number of malaria deaths in the whole of China. All the 14 malaria deaths between 2010 and 2015 in Henan Province were falciparum malaria cases imported from Africa; 12 of them had attended more than one medical institution before an authoritative and correct diagnosis was made; the 6.5 days spent may undermine the efforts based on Chinese 1-3-7 strategy [18, 19].

On the one hand, the notable mortality from imported malaria in Henan Province results from low awareness of severe perniciousness of malaria itself and lack of self-protective mentality and measures as well as wrong practice to treat malaria as common cold or fever empirically by malaria patients [20]. On the other hand, it is because of widespread misdiagnosis and malpractice on malaria patients in primary healthcare institutions [17, 18]. The robust multiple healthcare system in China once helped reduce indigenous malaria cases efficiently, but presently, it struggles to manage infrequent imported cases. It may need some targeted strategies to cope with the challenge of imported malaria. This study was designed to investigate the possible relationship between imported malaria cases and healthcare institutions based on imported malaria cases in Henan Province during 2012–2017 with a specific focus on the critical problem in imported malaria, as a precursor to targeted strategies on management of imported malaria cases.

Among the 371 imported malaria cases of this study, males were the majority, 366 (98.7%), and the median of age was 37 years, with a range of 17 to 67 years. There were no deaths in the sample during the study period. The malaria cases were mostly from P. falciparum: 319 (86.0%), and cases due to Plasmodium ovale, P. vivax and Plasmodium malariae were 34 (9.2%), 13 (3.5%) and 5 (1.3%), respectively (Table 1).

In the present study, the cases of malaria were imported from other countries where they had worked mainly as labourers and entrepreneurs; few cases were female and the majority of this sample were middle-aged and young [8]. Plasmodium falciparum is the most common species in African countries from where most malaria cases reported in Henan Province were imported. Patients infected by P. falciparum were more likely to be misdiagnosed and to develop complications in this study. Plasmodium falciparum is the most lethal form of parasite of human malaria, which develops rapidly with extreme and complex symptoms, sometimes followed by systemic complications that often result in death [28, 29].

When people with malaria return home from the countries where they were infected they normally plan a visit to certain healthcare facilities for treatment at their convenience, bearing in mind that there are always better medical services in healthcare institutions of higher administrative level in China. In advanced economies superior medical resources appear to be embedded. Because of the existence of marketing, China’s economy has always grown much stronger in areas of a higher administrative level. In contrast, there is disparity in the availability of health services and significant gaps in awareness of malaria and affordability by inhabitants at different administrative levels to the extent of severity of the illness in malaria patients [16, 30]. Therefore, for a number of malaria cases, provincial and municipal healthcare institutions served as their first option because many of them were near cities on their way home, or they lived in cities where better medical care gave them more trust and security. Among those cases living away from cities, in rural areas, they were inclined to frequent local healthcare institutions nearby. In rural areas, patients usually have a long way to go to county healthcare institutions. They treat their unexplained fevers as cold and take empirical medicine instead of visiting distant healthcare facilities, mostly because they are unaware of malaria [29]. County healthcare institutions are of higher profession and authority while village and private clinics are closest in rural areas, so the number of malaria cases initially diagnosed in these healthcare institutions were about the same as present sample. It is proven from the results that patients visiting private clinic, village clinic and township health centre had the shortest period from onset to initial diagnosis, while patients visiting county healthcare facilities had the longest period at first visit. The county healthcare institution of this study was relatively the least accessible but the most reliable healthcare institution in rural areas. It should be noted that the fewest patients were present at the township health centre with the shortest time interval because they maybe happened to live near the township.

It is noted that there are fewer misdiagnosed cases and complications formed at initial diagnosis in healthcare institutions of higher administrative level and that significantly more complications arose in malaria patients who are initially misdiagnosed. This may mean that misdiagnoses arising from poor performance in malaria diagnosis by healthcare institutions contributes to delays in treatment, which eventually leads to complications [31].

For initially misdiagnosed cases of malaria and patients with complications, a shorter time between onset and initial diagnosis was observed. On the one hand, most initially misdiagnosed patients appeared for initial diagnosis in healthcare institutions whose level of administration was lower than municipal level, where misdiagnosis of malaria was very common. In other words, the majority of patients who were initially misdiagnosed were from rural areas where medical services were worse and patients were used to visiting closer healthcare institutions so that the time interval between onset and initial diagnosis was shorter [32]. On the other hand, patients with severe malaria tended to visit healthcare institutions in a shorter time and they were more likely to be misdiagnosed. Cases with rapid onset as well as severe and complicated symptoms will seek medical help in shorter time. That means they have less time to visit a doctor but are more likely to be misdiagnosed and to develop complications. At the same time, as complications arise, it will be more difficult to diagnose patients correctly.

The decision tree model reinforces what was found and expresses it. Decision tree model of initial diagnosis defined township health centre, village clinic and private clinic as homogenous, with the largest proportion of initial misdiagnosis. It also listed municipal healthcare institutions and county healthcare institutions for initial diagnosis with a reasonable proportion of misdiagnosis. This suggests further that these healthcare institutions have similar capacity for malaria diagnosis. In the second decision tree model, dependent variable of complications developed, initial diagnosis became the most outstanding independent variable, which shows that initial diagnosis is significantly correlated with complications developed in malaria patients. Among those diagnosed correctly at the first visit, only one complication occurred in malaria cases receiving a final diagnosis within 24 h (node 5), while the remaining complications occurred in malaria cases that received the final diagnosis after longer periods (node 6). This may have shown that the final diagnosis and parasite confirmation in malaria cases with complications, relative to those without complications, would take more time. In other words, complications can make diagnosing and verifying the parasite correctly in patients with malaria more difficult. Besides, cases infected by P. falciparum accounted for most complications in malaria cases of node 6, suggesting a correlation between P. falciparum infection and complication in malaria patients.

International labourers from Chinese rural areas are the bulk of imported cases of malaria in China [33]. In imported malaria cases an extraordinary level of misdiagnosis and severe complications are observed. Poor performance in awareness, attitudes and practices of international labourers from rural areas, low capacity for malaria diagnosis in lower-level administrative healthcare institutions, and infrequency of malaria cases make these challenging characteristics of imported malaria in China [16, 20, 30]. A critical problem has been observed after a literature review of the challenge to tackle imported malaria in China [30, 34‐40]. It is well known that China’s strong healthcare system has wiped out a severe local malaria epidemic through mass intervention and specific strategies, which defines superiority in medical resources of China [41‐45]. Nevertheless, the system currently does not seem to be able to handle imported malaria effectively. This is because of the inaccessibility between unusual cases of imported malaria and advanced medical resources. To be exact, imported malaria cases have little knowledge about the association of their febrile symptoms with malaria. Meanwhile, healthcare institutions with advanced medical resources do not have capability to deal with countless febrile patients in remote rural areas. In this case, a clear travel history to malaria-endemic countries of a febrile patient is beneficial but often not available for some hidden causes [46]. There is a call for a definite link between imported malaria cases and healthcare institutions. There is firstly a proposed innovative internet-based system to make this connection a reality. A theoretical framework system recommended to the malaria department of the Ministry of Health in China consists of two sections. One is the database in the charge of Chinese multiple health departments to process fever information in the migrant population. In this way, febrile patients can be sorted to diagnose and treat any case of imported malaria. Another section is the request for every migrant’s mobile app in a way that, e.g., through WeChat which is the most prevalent social software, every migrant person could receive malaria-related information and communicate with corresponding healthcare centres on any febrile symptoms. This is per the law to eliminate malaria in the future. Specifically speaking, Chinese malaria department will launch a network system that combines communication tools or social software to register and manage migrant populations, with more emphasis on Chinese international labourers returning from Africa and Southeast Asia. In the network system, multiple healthcare institutions will keep in touch with their local migrant population. Any febrile cases must get in touch to report their symptoms to healthcare staff without any hesitation. Effective malaria diagnostic tests of high accuracy and drugs for therapy must be accessible in a short time, providing the means of transporting medical services to migrant febrile patients or sending patients to superior healthcare centres [30]. A panel on malaria diagnostic and treatment of high mobility and the combination of microscopy and RDT for diagnosis are recommended here [47]. To ensure the least burden caused by imported malaria, related laws and regulations will become a fact in the future. Any unintended adverse effects arising from incorrect or overdue practice by individuals and healthcare institutions must be detected. Daily data services to improve health literacy, imperative demands to high-risk population, and reliable and productive professional support could be effectively implemented within the system [30, 47, 48].

The pathway to controlling imported malaria and minimizing deaths is by linking malaria-related medical services to the limited migrant febrile population. Therefore, the proposed system would target a small population. Within the system, high quality malaria medical resources could be used to cope with a small number of migrant febrile cases intensively so its effectiveness could be unparalleled. It is an active, rather than passive, imported malaria management system [40] in which each migrant febrile patient communicates closely with and is in the charge of a local healthcare institution. More importantly, there should be a consensus that all Chinese citizens should undertake due obligation to reduce the burden of malaria and spare no effort to help achieve the goal of malaria elimination together with the Chinese Government, particularly in the context of imported malaria.

Inadequate seeking for medical care by imported malaria patients, and insufficient capacity to diagnose malaria by healthcare institutions of lower administrative level were identified as the major factors associated with complications of imported malaria cases in Henan Province, on which the crucial challenge of imported malaria is based. A web-based system combined with WeChat aimed at imported malaria patients was proposed that would possibly become a stimulation to alleviate the burden of imported malaria.