Epidemiological characteristics of Plasmodium malariae malaria in China: a malaria that should not be neglected post elimination

A total of 581 cases infected with P. malariae alone were reported from 2013 to 2022 in Chinese mainland with an overall slight increase, although it always represented a small percentage of the total cases reported nationally every year (1.3–3.9%) (Fig. 1), and 95.5% (555/581) of them are males (Table 1). The mean age of these cases was 40.6 ± 11.1 years old, ranging from 5 months old to 92 years old, and most of them (96.2%) were concentrated in 20–59 years old group (P < 0.001, Fisher’s Exact Test) (Table 1). And no asymptomatic cases and severe cases were reported.

Fig. 1figure 1

Proportion of malaria cases infected with Plasmodium malariae among the total malaria cases reported nationwide in China, 2013–2022

Table 1 Age and gender distribution of reported cases infected with Plasmodium malariae from 2013 to 2022 in ChinaTemporal distribution

Overall, there was no significant trend of cases reported by month, and no case was reported in April in 2015, July, August, September and November in 2020, March and May in 2021, and February, March and June in 2022, respectively. On a quarterly basis, relatively few cases were reported in the second quarter (April–June) (χ2 = 66.520, df = 27, P < 0.001) (Fig. 2).

Fig. 2figure 2

Quarterly distribution of the reported malaria cases infected with Plasmodium malariae reported in China, 2013–2022

Case diagnosis, confirmation and treatment

When the cases infected with P. malariae felt ill (fever, chill and headache), they first went to various medical and health institutions at different levels, including prefectural medical institutions (179), county medical institutions (165), provincial medical institutions (78), county center for disease control and prevention (CDCs) (45), village clinics (30), township health centers (28), individual clinics (22), prefectural CDCs (18), provincial CDCs (4), provincial entry-exit inspection and quarantine (EIQs) (3), prefectural EIQ (1), and no specific information on the institution of first visit was provided by the remaining 8 cases (Fig. 3a). Furthermore, they were mainly confirmed using microscopy by prefectural medical institutions (206), county medical institutions (135), provincial medical institutions (111), county CDCs (67), prefectural CDCs (30), provincial CDCs (13), township health centers (10), prefectural EIQ (3), provincial EIQs (2), and no specific information on the institution of confirmation was provided by the remaining 4 cases, respectively (Fig. 3b). However, only 379 cases (65.2%) were diagnosed as malaria on the first visit from 2013 to 2022 (χ2 = 133.243, df = 6, P < 0.001) (Table 2, Fig. 4a), and 413 cases (71.1%) were further confirmed as those infected with P. malariae (P = 0.002, Fisher’s Exact Test) (Table 2, Fig. 4b), and 153 cases (26.3%) were confirmed as those infected with other Plasmodium species, including P. vivax (70), P. falciparum (43), P. ovale spp. (28), untyping Plasmodium spp. (10), and mixed infections (2), respectively. Fortunately, all of the 581 cases infected with P. malariae were verified finally in the provincial reference laboratories for malaria diagnosis. Additionally, there were 403 and 175 patients who received inpatient and outpatient treatment, respectively, and three had unclear medical records. And most P. malariae cases were treated regularly according to the national treatment guidelines for P. malariae cases except for one case per year reported in 2016, 2017, 2018 and 2020.

Fig. 3figure 3

Distribution of reported cases infected with Plasmodium malariae at various health facilities nationwide in China, 2013–2022. a Case distribution in the first visit; b Case distribution when they were confirmed

Table 2 First diagnosis and confirmation of malaria case infected with Plasmodium malariae in various health facilities nationwide in China, 2013–2022Fig. 4figure 4

Distribution of malaria case infected with Plasmodium malariae diagnosed in the first visit and confirmation in various health facilities nationwide in China, 2013–2022. a Distribution of cases diagnosed as malaria cases in the first visit; b Distribution of cases confirmed as malaria cases infected with P. malariae

Case classification

Among all the reported cases infected with P. malariae alone from 2013 to 2022, most of them were imported cases (97.6%, 567/581), and 6 cases were indigenous cases, and 7 cases were recurrent cases, and one case was an induced case caused by blood transfusion (Additional file 1: Table S1).

Imported case

The imported cases (567) infected with P. malariae were from 41 countries in 8 regions (Fig. 5), and the highest number of cases came from Angola (122) in Central Africa (51.3%, 291/567) and Nigeria (75) in Western Africa (31.9%, 181/567) (Fig. 5). Meanwhile, these imported cases were distributed in 27 provinces (autonomous regions, municipalities) in China, and the largest number of reported cases were distributed in Jiangsu (93/567, 16.4%), Shandong (56/567, 9.9%), Henan (8.6%, 49/567), Zhejiang (6.9%, 39/567), Anhui (6.5%, 37/567) and Sichuan (6.5%, 37/567), respectively (Fig. 6, Additional file 2: Fig. S1).

Fig. 5figure 5

Country origins of the imported malaria cases infected with Plasmodium malariae reported in China, 2013–2022

Fig. 6figure 6

Provincial distribution of the imported malaria cases infected with Plasmodium malariae reported in China, 2013–2022

Indigenous case

A small outbreak of six indigenous malaria cases infected with P. malariae among forest goers from three villages (Baolong, Zhanan, Lixin) of Gaofeng Town in Sanya, Hainan Province, was reported from September to November 2015. All of them were male and aged from 19 to 40 years old, and were sequentially detected by blood smear microscopy and PCR in the passive case detection and active case detection.

Recurrent case

A total of 7 cases of recurrent malaria cases infected with P. malariae have been reported in Shanghai and Guangdong since 2014, and all of them were without recent history of travel to a malaria-endemic areas. Among them, one case was reported in Jing'an District in Shanghai in 2014 (Male, 75 years old); Six cases were reported from Guangdong Province, namely Zhongshan in 2014 (Female, 70 years old), Guangzhou in 2018 (Male, 75 years old), 2019 (Female, 75 years old) and 2021 (Female, 76 years old), Qingyuan in 2020 (Female, 92 years old), and Jiangmen in 2022 (Female, 67 years old), respectively. And all the cases of P. malariae recurrence were mainly determined based on the following aspects: (1) P. malariae was characterized using the laboratory diagnosis; (2) A case recalled having suffered from malaria previously; (3) Recent infection with P. malariae was excluded based on evidences from case investigation and focus investigation including no recent travel history to malaria-endemic areas, and P. malariae-negative results of malaria screening in neighboring population.

Induced case

An induced case (Male, 61 years old) infected with P. malariae due to the blood transfusion was confirmed by PCR and reported in Yangpu District in Shanghai in 2013.

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