PHWR Public Health Weekly Report

Japanese encephalitis (JE) is a zoonotic disease transmitted by mosquitoes [1]. This disease is caused by the JE virus, which belongs to the Flavivirus group that also includes the dengue virus, yellow fever virus, and West Nile virus. Although the main genotypes of the virus are geographically distributed, JE occurs primarily in Asian countries, and the initial symptoms are similar regardless of the genotype. On infection, most people experience mild symptoms, such as fever and headache; however, in rare cases, symptoms such as chills, muscle pain, and mental confusion can occur. In children, gastrointestinal pain and vomiting are the main early symptoms; convulsions are also common. Approximately 3 billion people are at a risk of infection with the JE virus, with approximately 20,000 new cases and 6,000 deaths reported each year globally. While the fatality rate ranges from 5% to 30%, approximately 30–50% of survivors experience various lifelong neurological complications, and only one-third of the patients fully recover [2,3].

Culex tritaeniorhynchus is the main mosquito species that transmits JE virus and is primarily distributed in East and Southeast Asian countries, including the Republic of Korea (ROK), China, Japan, Indonesia, and the Philippines. Although C. tritaeniorhynchus is the main vector, the JE virus has been isolated from over 30 mosquito species belonging to the genera Aedes, Anopheles, Armigeres, Culex, and Mansonia. However, it is unclear how many of these mosquito species are competent vectors [4].

In the ROK, the Division of Vectors and Parasitic Diseases of the Korea Disease Control and Prevention Agency (KDCA) conducts surveillance of the density of vector mosquitoes for JE virus to promptly identify the emergence and trends of the mosquitoes. On detection of C. tritaeniorhynchus, an alert for JE is issued. When one of the following conditions is met, a warning is issued for JE: (1) an average daily count of C. tritaeniorhynchus collected twice a week exceeding 500 specimens, constituting more than 50% of the total mosquito density; (2) isolation or detection of JE virus from collected mosquitoes; (3) reported cases of JE. When the criteria for issuing an alert and warning are met, public awareness is raised through nationwide surveillance program, and surveillance data are shared through the KDCA website. This project has been implemented since 1975 to establish effective measures for the prevention and control of JE, with the aim of improving public health. This report provides foundational data for the prevention and management of mosquito-borne diseases by analyzing the results of the 2023 JE surveillance program.

1. Mosquito Collection

The JE vector mosquito surveillance program was conducted in cooperation with nine Public Health and Environment Research Institutes at the city and provincial levels (Busan Metropolitan City, Gangwon Province, Chungcheongbuk Province, Chungcheongnam Province, Jeollabuk Province, Jeollanam Province, Gyeongsangbuk Province, Gyeongsangnam Province, and Jeju Province). In 2023, mosquitoes were collected from March 27 (13th week) to November 3 (44th week). From 2018 to 2023, black light traps were installed in the same manner at 11 collection sites (cowshed), and mosquitoes were collected twice a week. The mosquito index (i.e., trap index, which is the number of individuals/trap/day) was calculated.

2. Data Analysis

We compared and analyzed the weekly results of the mosquito collection uploaded on VectorNet, the KDCA’s vector-integrated surveillance system, with regional meteorological data collected from the Korea Meteorological Administration’s Meteorological Data Open Portal (https://data.kma.go.kr/cmmn/main.do). The mosquito distribution map was created using the ArcGIS 9.0 program (Environmental Research System Institute). We utilized the Inverse Distance Weighted Spatial Analyst Tool in the ArcGIS 9.0 software package for interpolation analysis based on the trap index.

3. Sharing of Surveillance Data

The density surveillance results for C. tritaeniorhynchus were updated every week (15–45 weeks) in the week following collection and were made available on the KDCA website (https://www.kdca.go.kr): “publications and statistics” → “(statistics) infectious disease outbreak information” → “weekly health and disease” → “major infectious disease statistics”.

1. Mosquito Collection Statistics

In 2023, a total of 221,311 mosquitoes belonging to 17 species were collected by nine Public Health and Environment Research Institutes from 11 collection sites. The trap index for all mosquitoes collected was 314.3. The dominant species in the collected mosquitoes was Aedes vexans nipponii, accounting for 45.3% (69,486 mosquitoes), followed by Anopheles sinensis, accounting for 27.9% (61,705 mosquitoes), and C. tritaeniorhynchus, accounting for 19.5% (43,251 mosquitoes) (Table 1). The mosquito index for C. tritaeniorhynchus, the primary vector of JE virus, was 61.4 (Figure 1). From 2019 to 2023, the overall trend showed a decrease in the number of individuals collected in 2020, followed by an increase in 2021. However, from last year, there has been a decrease again, with this year’s number of collections being similar to that of the previous year. Contrary to the overall mosquito occurrence trend, the population of C. tritaeniorhynchus decreased in 2021 and then increased in 2022, with a similar occurrence trend being observed in 2023

Figure 1. Total mosquito and vector mosquito prevalence trends (2019–2023)

Table 1 Total number of collected mosquitoes (%) by species in 2023

Genus	Species	No. of mosquitoes (%)
Aedes	Aedes vexans	100,242 (45.3)
	Aedes albopictus	206 (0.1)
	Aedes alboscutellatus	9 (<0.1)
	Aedes lineatopennis	7 (<0.1)
Ochlerotatus	Ochlerotatus koreicus	2,944 (1.3)
	Ochlerotatus togoi	595 (0.3)
	Ochlerotatus nipponicus	211 (0.1)
	Ochlerotatus hatorii	72 (<0.1)
	Ochlerotatus dorsalis	3 (<0.1)
Anopheles	Anopheles spp.	61,705 (27.9)
Culex	Culex tritaeniorhynchus	43,251 (19.5)
	Culex pipiens	7,113 (3.2)
	Culex orientalis	2,711 (1.2)
	Culex bitaeniorhynchus	90 (<0.1)
Armigeres	Armigeres subalbatus	1,910 (0.9)
Mansonia	Mansonia uniformis	240 (0.1)
Coquillettidia	Coquillettidia ochracea	2 (<0.1)
Total		221,311 (100.0)

2. Mosquito Density by Month and Week

Based on the collection results, a monthly distribution map of mosquito occurrence was created, which showed high density from May to September (Figure 2). Three species of mosquitoes (A. vexans nipponii, A. sinensis, and C. tritaeniorhynchus) accounted for 92.8% of all collected mosquitoes, and the main occurrence period differed depending on the species. The density of A. vexans nipponii increased from mid-May, that of A. sinensis from mid-June, and that of C. tritaeniorhynchus from August, with the highest overall density in August, wherein all three species also had a relatively high density.

Figure 2. Monthly incidence of total mosquiotes in 2023

When compared by week, the trap index was considerably reduced in the first week of July, which showed the highest average density across 2019–2023 and in 2022 (Figure 3). Considering the initial occurrence of C. tritaeniorhynchus, the primary vector for JE virus, by region and week, its appearance across different regions differed: it appeared by Week 13 in Busan Metropolitan City, by Week 14 in Jeju Province, by Week 16 in Gyeongsangnam Province, by Week 27 in Gyeongsangbuk Province, by Week 28 in Gangwon Province, Chungcheongbuk Province, and Jeollanam Province, by Week 29 in Jeollabuk Province, and by Week 30 in Chungcheongnam Province (Table 2). Hence, there was a regional difference in the timing of appearance of C. tritaeniorhynchus, with later appearances in the northern regions (Figure 2).

Figure 3. Weekly incidences of total mosquitoes and vector mosquitoes in 2023

Table 2 First collected week of Culex tritaeniorhynchus by region (2021–2023)

Region	First week of collected C. tritaeniorhynchus
	2021	2022	2023
Gangwon Province	35	29	28
Chungcheongbuk Province	30	30	28
Chungcheongnam Province	34	32	30
Jeollabuk Province	23	30	29
Jeollanam Province	23	26	28
Gyeongsangbuk Province	32	27	27
Gyeongsangnam Province	25	17	16
Busan Metropolitan City	14	15	13
Jeju Province	14	16	14

3. Issuance of JE Alerts/Warnings

In 2023, JE alerts and warnings were issued nationwide on March 23rd following the confirmation of collection of C. tritaeniorhynchus in Busan Metropolitan City and Jeju Province by the surveillance sites of a vector surveillance program, “Regional climate change vector surveillance hub centers” operated by the KDCA’s Division of Vectors and Parasitic Diseases, on March 22nd. Another JE warning was issued nationwide on July 26th following the confirmation of C. tritaeniorhynchus mosquitoes in Busan Metropolitan City, which accounted for 91.4% of all mosquitoes collected (1,056 of 1,155 individuals).

In 2023, the total number of mosquitoes collected from nine Public Health and Environment Research Institutes (11 collection points) in the ROK decreased by 4.9% when compared to 2022; similarly, the number of vector mosquitoes decreased by 6.4% when compared to 2022. In the same year, a total of 10 typhoons occurred (with an average of 11 typhoons per year [1993–2023]). Among them, the sixth typhoon “Khanun” affected ROK, which experiences an average of 2.5 typhoons every summer, bringing heavy rain and strong winds on the 9th and 10th of August, as per Korea Meteorological Agency’s summer climate characteristics press release. This meteorological event is thought to be caused by the sudden decrease in the number of total and vector mosquitoes during Week 32 of 2023, which is generally the peak period for mosquito proliferation in summer. The reduced density of mosquitoes in Week 27 of 2023 (the period with the highest mosquito density on average and with the highest density in 2022) may be attributed to the average temperatures of the previous two weeks, i.e., Week 26 and Week 25, being 2.3°C and 2.7°C lower, respectively. Additionally, mosquito eggs and larvae are significantly affected when daily precipitation exceeds 75 mm (heavy rainfall) or when the total precipitation over 15 days exceeds 150 mm [5]. In 2023, the average number of rainy days per month was 13.3 days, and the monthly average precipitation was 296.1 mm during summer (June–August). The higher precipitation and number of rainy days in 2023, totaling 40.0 days during summer, compared to that in the previous year (39.1 days) and the average year (35.1 days), are speculated to have led to the observed decrease in mosquito occurrence in 2023. On the contrary, according to data from the Korea Meteorological Administration, during September, the temperature was 22.6℃, which was 2.1℃ higher than the average (1993–2023), marking the highest recorded temperature in autumn since 1973. Additionally, warm southwest winds blew along the edge of the North Pacific High Pressure during the mid to late September, which also contributed to the high temperatures in autumn. These conditions are believed to have led to higher mosquito densities in autumn owing to the difficulty in mosquito breeding and larval development during summer as a result of high rainfall.

Owing to effects of climate change, such as tropicalization and environmental changes, the timing of issuing JE alerts and warnings has advanced by approximately 3 months for alerts and 1 month for warnings when compared to that in 1975. The timing of issuing alerts, specifically, is thought to represent the increase in activity periods of ectothermic animals, such as insects, due to climate warming [6]. Therefore, it is necessary to expand the monitoring scope for JE vector mosquitoes and ensure continuous and uniform surveillance to promptly identify the trends in occurrence and density of these mosquitoes in response to various environmental and ecological changes caused by climate change.

Ethics Statement: Not applicable.

Funding Source: None.

Acknowledgments: None.

Conflict of Interest: The authors have no conflicts of interest to declare.

Author Contributions: Conceptualization: BEN, HWK, JWJ, HIL. Data curation: BEN, SES, HWK. Formal analysis: BEN, HWK. Writing – original draft: BEN. Writing – review & editing: BEN, HWK, JWJ, HIL.