Vital Surveillances: Malaria Deaths — China, 2011–2020

Introduction: The malaria deaths (MDs) caused by imported Plasmodium falciparum has become a great challenge. This article analyzed MDs in China in 2011−2020 to provide evidence-based data for further strategies and interventions adjustment.

Methods: Individual data via the National Notifiable Disease Reporting System (NNDRS) in 2011−2020 were collected. The Plasmodium species, case classification, temporal and spatial distribution, and source of MDs were analyzed to explore MD characteristics. The Parasitic Diseases Information Reporting Management System (PDIRMS) of MDs in 2013−2020 which explored clinical symptom and treatment was also collected and analyzed.

Results: A total of 165 MDs with a mortality rate of 0.5% were recorded in the NNDRS from 2011 to 2020. Among them, 164 (99.4%) died due to imported malaria cases, 1 (0.6%) died of indigenous case reported in Yunnan in 2013. The number of MDs showed a decreasing trend from 2011 (n=30) to 2020 (n=6). The MDs consisted of 160 (97.0%) P. falciparum cases, 1 (0.6%) mixed infection case, and 4 (2.4%) clinical diagnosed cases. The MDs were mainly reported in Guangdong (n=18, 10.9%), Sichuan (n=17, 10.3%), Beijing (n=15, 9.1%) and Henan (n=15, 9.1%). The PDIRMS had reported 121 MDs from 2013−2020, and 46.3% (n=56) of MDs exhibited severe brain damage, and most of the patients (n=95, 78.5%) were administrated by artemisinin combination therapy injection form.

Conclusions: The total MDs decreased in China, and a delay in diagnosis and treatment is the main causes of MDs. Therefore, two actions are needed to prevent MDs, including improving health education for key populations such as migrant workers who come to and return from endemic regions and maintaining malaria diagnosis and treatment capabilities of clinicians in medical facilities.

China has eliminated indigenous malaria and reached this milestone for 4 consecutive years since 2017 (1-2). However, with globalization and economic integration, an increasing number of people come to or return from Africa and Southeast Asia, which also make imported malaria as a major challenge to malaria post-elimination stage in China (3-5). Severe malaria infections, or even fatalities, that are mainly caused by imported Plasmodium falciparum (P. falciparum), would be catastrophic if diagnosis and treatment could not be carried out promptly.

Therefore, the objective of this study was to characterize the epidemiological status of malaria deaths (MDs) and the clinical symptoms and treatments for deaths from 2011 to 2020, aiming to provide evidence-based data that could support the adjustment of appropriate control strategies and activities during the malaria post-elimination stage in China.

Data from 31 provincial-level administrative divisions (PLADs) via the National Notifiable Disease Reporting System (NNDRS) were collected and carefully reviewed from January 1, 2011 to December 31, 2020. The NNDRS, which was set up in 2004 after the severe acute respiratory syndrome (SARS) outbreak, is a standardized platform that provides healthcare systems nationwide with the ability to detect, analyze, prevent, and respond to any communicable diseases in the country. The clinically diagnosed cases referred to individuals with malaria-related symptoms [fever (axillary temperature ≥ 37.5 °C), chills, severe malaise, headache, or vomiting] at the time of examination, and laboratory-confirmed cases referred to clinical cases confirmed by microscopy, polymerase chain reaction (PCR), or rapid diagnostic tests (RDT) in the laboratory, and both types of cases were included in this analysis. The clinical symptoms and treatments of all MDs from 2013 to 2020 were collected from the Parasitic Diseases Information Reporting Management System (PDIRMS). Data from Hong Kong, Macao, and Taiwan were excluded in this study. Individual information including Plasmodium species, case classification, source of death cases, intervals from onset to diagnosis, intervals from onset to death, and treatment were used to analyze MD characteristics. The statistical analysis was evaluated by trend chi-squared tests (SPSS, version 21.0, IBM Corp.), and P<0.05 was considered as statistical significance.

A total of 165 MDs with a fatality rate of 0.54% were recorded in the NNDRS from 2011 to 2020 (Table 1). Among them, 164 (99.4%) MDs were due to imported malaria cases, and 1 death was an indigenous case (2013 in Yunnan). The number of MDs decreased from 2011 (n=30) to 2020 (n=6), a result which was statistically significant (evaluated by trend chi-squared test, χ²=322.153, P<0.001). The MDs consisted of 160 (97.0%) P. falciparum cases, 1 (0.6%) mixed infection case (2012 in Xinjiang), and 4 (2.4%) clinically-diagnosed cases. Most of the MDs (n=143, 86.7%) were reported in 22 endemic PLADs, and others (n=22, 13.3%) were reported in 5 non-endemic PLADs. The MDs were mainly reported in Guangdong (n=18, 10.9%), Sichuan (n=17, 10.3%), Beijing (n=15, 9.1%), and Henan (n=15, 9.1%) (Table 2). The distribution of MDs has been shrunken for reported cases from 14 PLADs in 2011 to 3 PLADs in 2020. The highest number of MDs was observed in the age group of 46 to 50 (n=32, 19.4%), followed by the age group of 40 to 45 (n=29, 17.6%). The highest number of MDs occurred in 2011 (n=30, 18.2%). The temporal distribution showed that MDs was reported throughout the whole year and monthly distribution showed that the highest number of MDs was reported in January (n=27, 16.4%) and February (n=23, 13.9%) (Figure 1). The MDs (n=156, 94.5%) were reported in hospitals and CDCs (n=9, 5.5%). In addition, the MDs were mainly reported by facilities at the prefecture level (n=95, 57.6%), at the provincial level (n=54, 32.7%), and at the county level (n=16, 9.7%). The average medium of interval from onset to diagnosis was 7 days, and the average medium of interval from onset to death was 8 days. Most of the MDs were from people of Chinese nationality (n=162, 98.2%).

The MDs due to imported cases were from 30 countries and 2 continents. Among them, 150 cases (90.9%) were from Africa and mainly from Central (n=59, 35.8%) and West Africa (n=47, 28.5%), including Angola (n=27, 16.4%), Nigeria (n=17, 10.3%), and Mozambique (n=10, 6.1%) (Table 3). For the MDs from Southeast Asia, they were mainly from Myanmar (n=8, 4.8%), Cambodia (n=1, 0.6%), and Indonesia (n=1, 0.6%).

The PDIRMS showed that among 121 MDs reported from 2013 to 2020, 46.3% (n=56) of them exhibited severe brain damage and 19.0% of them exhibited (n=23) severe liver and kidney damage. Most of the patients (n=95, 78.5%) were administrated by artemisinin combination therapy injection form.

Malaria mortality has declined over the past decades in China. The findings in this study revealed that most of the deaths were identified as imported malaria cases in returning migrant workers from Africa, and the findings were similar to a previously reported study (6). This result was consistent with expectations as P. falciparum was widespread in Africa, and Central and West Africa were the main source regions of imported deaths, which were regions with high disease burden of malaria mortality as reported by the World Health Organization (WHO) (7).

The interval from onset to diagnosis was 7 days in this study, which was longer than that reported in other non-endemic countries, whose median diagnosis delays were 4 or more days (8). Reasons that are likely to cause delays from onset to diagnosis are as follows. First, the patients failed to recognize the harm of malaria to the human body, which led to poor awareness of medical treatment. After the appearance of symptoms such as chills and fever, patients did not pay attention on them. They often obtained infusions in small clinics and even self-administered medication to relieve symptoms, which could lead to delays in diagnosis and treatment, worsen conditions, and even death. These factors were found in some MDs reported recently in Beijing, Sichuan, Shanghai, Jiangsu, and Shandong (9-13).

Second, the clinicians had insufficient experience in the diagnosis and treatment of malaria, and some of them did not take the initiative to ask the patient’s epidemiological history, so patient who had symptoms of P. falciparum could not be promptly diagnosed. Third, low-level hospitals for first visits were also main factors influencing malaria deaths. In this study, 47.9% of MDs were first diagnosed in county-level hospitals or below, which need to be strengthened on capacity building, particularity for malaria diagnosis and treatment. A study by Tu et al. has also proved this point by learning the experience and lessons on 16 MDs reported in China (14). Finally, most patients who were infected with P. falciparum were diagnosed with malaria abroad in private clinics had previously received improper treatments such as aspirin, which added the risk of recurrence of P. falciparum when they returned from African countries. This was similar to P. vivax and P. ovale. For example, in 2014, 78.6% of all imported P. vivax and P. ovale in Guangxi were individuals who had been given aspirin instead of antimalarial agents (15).

The results indicated that MDs occurred in returning migrant workers from January and February because most of the migrant population came back from abroad at this period due to the Chinese Spring Festival, and delays in diagnosis and treatment were the main causes of MDs. Since imported P. falciparum was now reported in every PLAD in China, timely detection, proper treatment, and deaths prevention caused by imported P. falciparum were major challenges faced by post-elimination stage in China. Therefore, some strategies and interventions should be carried out as follows: 1) health education through cooperation with customs and CDCs for the targeted populations such as migrant workers who come to and return from endemic regions; 2) maintain malaria diagnosis and treatment capabilities of clinicians in medical facilities above county levels, especially in the COVID-19 prevention and control process since both malaria and COVID-19 harbored the same clinical symptom at the initial onset stage; and 3) improve the ability to treat severe malaria cases. Expert panels at the national and provincial level could use these recommendations derived from tracking the reasons for MDs and provide suggestions for preventing MDs caused by imported malaria.

The study was subject to some limitations. Not all MDs were well recorded with the exact epidemiological information in 2011–2020. The study still has 5 unknown MDs imported from abroad. In addition, not all MDs were confirmed in the laboratory as 4 clinically diagnosed cases were found in this study.

Figure 1. 

Temporal distribution of malaria deaths (MDs) in China, 2011–2020.

Acknowledgement: Provincial and county-level CDCs in China.

Conflict of interest: No conflicts of interest were reported.