Abstract
The Division of Vectors and Parasitic Diseases of the Korea Disease Control and Prevention Agency has been conducting malaria vector mosquitoes (Anopheles spp.) since 2009 for eradicating malaria in the Republic of Korea. The density of mosquito vectors and Plasmodium vivax in mosquitoes detection were investigated from April to October 2022 at 50 locations in high-risk malaria areas (Incheon, Gyeonggi, and parts of Gangwon). In 2022, the trap index (TI; mosquitoes/trap/night) of mosquito vectors was 68, which was lower by 34.6% and 27.7% compared to the average year (2017–2021) and 2021, respectively. The highest density of mosquito vectors over the year 2022 was a TI of 8 in the 33rd week, which was five weeks later than that of the year 2021, where the highest density was observed in the 28th week (TI=10). The peak density of malaria vector mosquitoes occurred in the 27th week (end of June) of 2022 in Gyeonggi, the 33rd week (August) in Gangwon, and the 37th week (early September) in Incheon. The highest density of mosquito vectors was observed in Paju (TI=195) followed by Cheorwon (TI=119), and Yang-gu (TI=88). In addition, one pool of P. vivax (with a minimum infection rate of 0.07) was detected in the 37th week of 2022, which was five weeks later than that of 2021. The steady occurrence of malaria vectors and the appearance of positively infected mosquitoes demands caution against malaria infection and continuous mosquito surveillance. Subsequently, these data are important for implementing effective malaria prevention strategies, such as early warning and alert systems.
Keywords: Key words: Malaria vector mosquito, Plasmodium vivax, Monitoring, High-risk region
Key messages
① What is known previously?
Plasmodium vivax malaria is endemic in northern part of Incheon, Gyeonggi, Gangwon and more than 80% of malaria cases occurred in this area.
② What new information is presented?
Plasmodium vivax was detected in mosquitoes in week 37. This site showed 17.1% increasing of mosquito population with 2021.
③ What are implications?
For three years, the percentage of malaria vector mosquitoes collected from military areas was higher than civilian areas. Therefore, malaria prevention and mosquito control are likely to be necessary in military section. With improving of COVID-19, it is expected to increase contact between mosquitoes and patients. Therefore, local health center should implement effective control and strive to personal protection.
Introduction
Malaria is an acute febrile disease caused by infection with the protozoan genus Plasmodium. Humans are definitive hosts and become infected when infected sporozoites from female anopheline mosquitoes’ salivary glands enter the bloodstream while they are probing humans for blood. Humans can contract five malaria species: Plasmodium falciparum, P. vivax, P. malariae, P. ovale, and P. knowlesi. The domestic indigenous malaria in the Republic of Korea (ROK) is P. vivax, occurring in Incheon, Gyeonggi, and Gangwon, with infections primarily occurring near the Military Demarcation Line [1].
Among the mosquito genus Anopheles, the primary biological vector of malaria, eight species (i.e., Anopheles sinensis, An. kleini, An. lesteri, An. pullus, An. belenrae, An. sineroides, An. koreicus, and An. lindesayi) inhabit the ROK, whereas An. koreicus and An. lindesayi have not yet been reported as malaria vectors [2].
Since 2009, the Division of Vectors and Parasitic Diseases of the Korean Disease Control and Prevention Agency has partnered with the Institute of Health and Environment (Incheon Metropolitan City, northern Gyeonggi Province, and Gangwon Province) and health centers to continue monitoring malaria vector mosquitoes in malaria risk areas. Since 2019, the Ministry of National Defense has also been collaborating on investigations of vector and P. vivax in mosquito densities.
Through this project, the seasonal and regional occurrence densities of malaria vector mosquitoes are investigated annually and used in determining the timing of extermination. Efforts are being made to actively release the investigation results of P. vivax malaria protozoal infection rates in mosquitoes to improve strategies to eradicate malaria.
Methods
Mosquito collection and the investigation of malaria vector mosquitoes were carried out with the help of local health centers, county hospitals, military preventive medicine services, and the Institute of Health and Environment.
1. Mosquito collection
The 2022 density investigation of malaria vector mosquitoes was conducted at 36 sites in civilian areas in Incheon, Gyeonggi, and Gangwon, and 14 sites in the military areas where patients had been or were likely to be identified (Table 1). The malaria vector mosquito collection was carried out seven days a week in civilian areas using black light traps for seven months of the year (April–October), and two days a week using light-emitting diode (LED) traps in military bases located in low-temperature mountainous areas for five months (May–September), taking into account the mosquito season and regional characteristics.
Table 1. Malaria vector mosquitoes collecting site in 2022.
| Category | Institutions | Collecting site | Malaria vector population | Plasmodium vivax infection |
|---|---|---|---|---|
| Incheon (12) | Institute of Health and Environment Research (5) | Unnam-dong, Jung-gu | ⊙a) | ○ |
| Seonjuji-dong, Gyeyang-gu | ○ | ○ | ||
| Bupyeong-dong, Bupyeong-gu | ○ | ○ | ||
| Yeonhui-dong, Seo-gu | ○ | ○ | ||
| Baekseok-dong, Seo-gu | ○ | ○ | ||
| Ganghaw Public Health Center (7) | Sungnoe-ri, Songhae-myeon | ⊙a) | ○ | |
| Soljeong-ri, Songhae-myeon | ⊙a) | ○ | ||
| Geumwol-ri, Seonwon-myeon | ⊙a) | ○ | ||
| Seongmo-ri, Samsan-myeon | ⊙a) | ○ | ||
| Daeryoung-ri, Gyodong-myeon | ⊙a) | ○ | ||
| Daesan-ri, Ganghwa-eup | ⊙a) | ○ | ||
| Wolgot-ri, Ganghwa-eup | ⊙a) | ○ | ||
| Gyeonggi (16) | Gimpo Public Health Center (4) | Sau-dong | ⊙a) | ○ |
| Magok-ri, Haseong-myeon | ○ | ○ | ||
| Gunha-ri, Wolgot-myeon | ○ | ○ | ||
| Yulsaeng-ri, Daegot-myeon | ○ | ○ | ||
| Paju Public Health Center (4) | Beopheung-ri, Tanhyeon-myeon | ⊙a) | ○ | |
| Josan-ri, Gunnae-myeon | ○ | ○ | ||
| Majeong-ri, Munsan-eup | ○ | ○ | ||
| Baegyeon-ri, Gunnae-myeon | ○ | ○ | ||
| Goyang Public Health Center (1) | Daejang-dong, Deogyang-gu | ⊙a) | ○ | |
| Dongducheon Public Health Center (1) | Habongam-dong | ⊙a) | ○ | |
| Uijeongbu Public Health Center (1) | Sangok-dong | ⊙a) | ○ | |
| Pocheon Public Health Center (1) | Giji-ri, Sinbuk-myeon | ⊙a) | ○ | |
| Yeoncheon Healthcare (4) | Daegwang-ri, Sinseo-myeon | ⊙a) | ○ | |
| Namgye-ri, Gunnam-myeon | ○ | ○ | ||
| Samgot-ri, Jung-myeon | ○ | ○ | ||
| Nogok-ri, Baekhak-myeon | ○ | ○ | ||
| Gangwon (8) | Cheorwon Public Health Center (2) | Daema-ri, Cheorwon-eup | ⊙a) | ○ |
| Haksa-ri, Gimhaw-eup | ○ | ○ | ||
| Hwacheon Healthcare (1) | Sineup-ri, Hwacheon-eup | ⊙a) | ○ | |
| Inje Public Health Center (1) | Deoksan-ri, Inje-eup | ⊙a) | ○ | |
| Yanggu Public Health Center (1) | Guam-ri, Nam-myeon | ⊙a) | ○ | |
| Chuncheon Public Health Center (2) | Jinae-ri, Sinbuk-eup | ○ | ○ | |
| Jungang-dong | ○ | ○ | ||
| Goseong Public Health Center (1) | Myeongpa-ri, Hyeonnae-myeon | ⊙a) | ○ | |
| Troop (14) | Gimpo (1) | Troop A | ○ | ○ |
| Paju (6) | Troop A | ○ | ○ | |
| Troop B | ○ | ○ | ||
| Troop C | ○ | ○ | ||
| Troop D | ○ | ○ | ||
| Troop E | ○ | ○ | ||
| Troop A-1b) | 50 | 50 | ||
| Yeoncheon (4) | Troop A | ○ | ○ | |
| Troop B | ○ | ○ | ||
| Troop C | ○ | ○ | ||
| Troop D | ○ | ○ | ||
| Cheorwon (3) | Troop A | ○ | ○ | |
| Troop B | ○ | ○ | ||
| Troop C | ○ | ○ | ||
| Goseong (1) | Troop A | ○ | ○ | |
| Total | 50 | 50 | 50 |
a)Same collecting site in 2009-2022 (20 points). b)Paju A-1(additional area) is a LED trap added at a different location within Paju unit A and is not included in the malaria data.
At each site, the collected mosquitoes were identified to genus level using stereo microscopes, and only female mosquitoes were counted. The results were communicated to the Division of Vectors and Parasitic Diseases of Korea Disease Control and Prevention Agency through VectorNet (http://is.kdca.go.kr), within the integrated disease and health management system.
2. Investigation of P. vivax in mosquitoes
The presence of P. vivax in vector mosquitoes was examined through gene testing (nested polymerase chain reaction) at the Institute of Health and Environment (Incheon, north Gyeonggi, and Gangwon) and the military preventive medicine services [3]. Suspected positive samples were verified by the Division of Vectors and Parasitic Diseases of Korea Disease Control and Prevention Agency.
3. Provide surveillance information
Density estimates of vector mosquitoes and data on the presence of protozoa were updated weekly on the homepage of the Korea Disease Control and Prevention Agency (http://www.kdca.go.kr) → Periodicals·Statistics → (Statistics) Domestic Infectious Disease Occurrence → Public Health Weekly Report → Major Infectious Disease Statistics. This information is divided by province and includes information for weeks 14–44.
Results
The data of the 2022 density investigation of malaria vector mosquitoes was converted into a trap index (TI) (TI=number of mosquitoes collected/number of light traps/number of collection days), and compared with the data from 2021 and a average year (average of data from 2017 to 2021). The sum of the weekly TI of Anopheles spp. in 2022 was 68, a 34.6% decrease from 104 in a average year and a decrease of 27.7% from 94 in 2021. In addition, Anopheles spp. accounted for 27.5% of the total mosquitoes in 2022, a decrease of 7.1% and 7.8% compared with that of a average year and 2021, respectively (Table 2).
Table 2. Ttrap index (TI) of collected mosquitoes in 2022.
| Category (yr) | Collecting site | Total mosquito | Malaria vector mosquitoes | Proportion of malaria vector mosquitoes (%) | Avg of malaria vector mosquitoes TIa) | ||||
|---|---|---|---|---|---|---|---|---|---|
| Accumulate of weekly TIa) | Variation (%) | Accumulate of weekly TIa) | Proportion of change (%) | ||||||
| Average (2017–2021) | – | 301 | – | 104 | – | 34.6 | 3.4 | ||
| 2021 | 50 | 266 | – | 94 | – | 35.3 | 3.0 | ||
| 2022 | 50 | 247 | Average year | 17.9% decrease | 68 | Average year | 34.6 down | 27.5 | 2.2 |
| Previous year | 7.1% decrease | Previous year | 27.7 down | ||||||
a)TI=No. of mosquitoes/traps/days.
Mosquitoes can survive at temperatures between 15 and 35℃ [4], with the number of Anopheles spp. increasing rapidly at 20℃ and appearing most frequently at an average temperature of 26.2℃ [5]. The average temperature between weeks 27 and 33℃, coinciding with the occurrence peak in 2022, was measured at approximately 25℃ (Figures 1, 2) [6], with the mean maximum temperature during this period confirmed as an appropriate temperature for mosquito occurrence, at around 28℃. Furthermore, it is estimated that the precipitation 2–3 weeks prior to weeks 27 and 33, when the peak occurrence of mosquitoes was observed, had created a temporary larval habitat, providing a suitable environment for mosquito eggs and larvae to develop [7]. However, in the summer of 2022, there was more than 100–300 mm of heavy rainfall per day in the areas of Incheon, Gyeonggi, Gangwon, and Seoul [8], and it is thought that the overall collection of mosquitoes decreased due to various factors, including disturbance in spawning behavior and the loss of eggs and larvae.
Figure 1. Malaria vector mosquitoes density in 2022 (weekly, 50 collection sites).
Figure 2. Average temperature, daily precipitation and malaria vector TI (Trap Index) in 2022.
Data from KMA National Climate Data Center 2015 (https://data.kma.go.kr/data/grnd/selectAwsRltmList.do?pgmNo=56) [7].
The mean vector mosquito TI per area was 57 for Gyeonggi, 26 for Gangwon, and 22 for Incheon, and the ratio of vector mosquitoes to total mosquitoes was 49.2%, 43.2%, and 13.1% for the three areas, respectively. Among all of the collection sites, Paju in Gyeonggi showed the highest occurrence of malaria vector mosquitoes, followed by Cheorwon and Yanggu in Gangwon, and Ganghwa in Incheon (Figure 3). In particular, most of the vector mosquitoes were collected in Josan in Paju, accounting for 41.2% of the vector mosquitoes in the entire collection area. Chosan is within the demilitarized zone (DMZ), where civilians are prohibited from entering, and most of it is used as agricultural land. It is assumed that water pools such as rice paddies [7] become a habitat for mosquito larvae, and the occurrence of mosquitoes is consequently high in this area.
Figure 3. Accumulation of malaria vector mosquitoes TI in 2022 (include troop).
The accumulation of trap index (TI) in each collecting site (Gangwon: 12, Gyeonggi: 26, Incheon: 12).
The investigation of malaria vector mosquitoes in 2022 showed that one pool-positive mosquitoes appeared in Cheorwon. The 2022 investigation of malaria vector mosquitoes found one pool, as in 2021, but the minimum infection rate increased by 16% to 0.07.
The period of highest occurrence of malaria vector mosquitoes was found to vary by region (Figure 4). Malaria vector mosquitoes in the Gyeonggi region peaked in week 27 (end of June), Gangwon in week 33 (August), and Incheon in week 37 (beginning of September). These monitoring results can be used not only as information for preventing and responding to malaria and exterminating malaria vector mosquitoes by period but also as important basic data to predict the future occurrence of malaria vector mosquitoes.
그림 4. Sum of TI (Trap Index) for total and malaria vector mosquitoes by week in Gyeonggi, Gangwon, and Incheon.
Although the mean annual vector mosquito TI in this project was higher in the civilian (2.5 mosquitoes) than in military areas (1.6 mosquitoes), the ratio of vector mosquitoes collected was 64.1% in the military areas, more than twice as high as the 28.1% recorded in the civilian areas (Table 3). In addition, among the mosquitoes collected in military areas during the last three years, malaria vector mosquitoes accounted for more than 60% of the total mosquito population. Particularly, despite the decline in the number of vector mosquitoes in 2022, their percentage in military areas still remained above 60%. These results suggest a high likelihood of exposure to malaria vector mosquitoes in military areas, and more thorough preventive measures such as personal defense are needed in military areas.
Table 3. Comparison of No. of mosquito population in civilian and troop areas compared to 2021 in 2022.
| Division | Total mosquitoes | Malaria vector mosquitoes | Proportion of malaria vector mosquitoes (%) | Annual mosquitoes Trap index |
|---|---|---|---|---|
| 2022 | ||||
| Civilian | 65,919 | 18,542 | 28.1 | 2.5 |
| Troop | 1,582 | 1,014 | 64.1 | 1.6 |
| Total | 67,501 | 19,556 | 29.0 | 2.3 |
| 2021 | ||||
| Civilian | 71,617 | 24,946 | 34.8 | 3.2 |
| Troop | 1,718 | 1,146 | 66.7 | 1.9 |
| Total | 73,335 | 26,092 | 35.6 | 3.0 |
Discussion
In 2022, the density of vector mosquitoes decreased compared to that in average year (2017–2021) and 2021. Because mosquitoes are strongly affected by weather conditions such as temperature and precipitation [9, 10], it is presumed that mosquito activity and spawning were hindered and eggs and larvae were lost, resulting in a decreased number of mosquitoes in weeks 27 and 33 of 2022, when there was heavy rainfall.
The 2022 investigation of malaria vector mosquitoes detected positive for P. vivax in week 37, and it is estimated that temperatures adequate for mosquito development were maintained due to rising temperatures, and the mosquitoes were detected somewhat later than the average appearance interval. In addition, although there was only one positive mosquito pool sampled in 2022 and 2021, continuous and long-term caution against malaria vector mosquitoes is expected to be necessary to prevent mosquito bites, as more than one positive mosquito has been consistently identified in the last three years.
The number of malaria patients increased in 2022 despite a decline in vector mosquitoes. This can be questioned in connection with a World Health Organization report that suggested a 22.8% increase in malaria cases in 2021 compared to that in 2020 in North Korea [11]. Therefore, special attention to mosquito bites is required in the border area, as it is a malaria risk area, and further detailed analysis of mosquito densities by collection site is needed.
As in 2021, the number of malaria vector mosquitoes in 2022 was higher in military than civilian areas. The black light traps and LED traps used in civilian areas and military bases have similar Anopheles spp. collection rates [12], and it is estimated that a high density of mosquitoes was observed in military areas because they provide a better environment for vector mosquito habitation than the civilian areas do. Therefore, more caution concerning contact with mosquitoes is required in military areas (near the DMZ) where there are many outdoor activities, and it is crucial to establish effective malaria infection prevention measures using periodic monitoring information on mosquito populations and protozoal infection rates in malaria risk areas, including military bases.
The Division of Vectors and Parasitic Diseases of Korea Disease Control and Prevention Agency uses mosquito monitoring information updated weekly to combat malaria by informing the public with malaria alerts, warnings, and press releases and is planning on promoting infection prevention awareness and personal protection measures to ensure the successful eradication of malaria.
Acknowledgments
None.
Declarations
Ethics Statement: Not applicable.
Funding Source: None.
Conflict of Interest: The authors have no conflicts of interest to declare.
Author Contributions: Conceptualization: HIS, JWJ, HIL. Data curation: BGH, HIS. Formal analysis: BGH, HIS. Supervision: HIS, JWJ, HIL. Writing-original draft: BGH. Writing-review & editing : BGH, HIS, JWJ, HIL.
REFERENCES
- 1.Korea Disease Control and Prevention Agency, author. 2022 Malaria management guidelines. Korea Disease Control and Prevention Agency; 2022. [DOI] [Google Scholar]
- 2.Yoo DH, Shin EH, Park MY, et al. Mosquito species composition and Plasmodium vivax infection rates for Korean army bases near the demilitarized zone in the Republic of Korea, 2011. Am J Trop Med Hyg. 2013;88:24–8. doi: 10.4269/ajtmh.2012.11-0755. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Snounou G, Viriyakosol S, Zhu XP, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61:315–20. doi: 10.1016/0166-6851(93)90077-B. [DOI] [PubMed] [Google Scholar]
- 4.Agyekum TP, Botwe PK, Arko-Mensah J, et al. A systematic review of the effects of temperature on Anopheles mosquito development and survival: implications for malaria control in a future warmer climate. Int J Environ Res Public Health. 2021;18:7255. doi: 10.3390/ijerph18147255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Lim AY, Cheong HK, Chung Y, Sim K, Kim JH. Mosquito abundance in relation to extremely high temperatures in urban and rural areas of Incheon Metropolitan City, South Korea from 2015 to 2020: an observational study. Parasit Vectors. 2021;14:559. doi: 10.1186/s13071-021-05071-z.dd59b8e149bc48718b2f3dc4af731bcc [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.KMA National Climate Data Center, author. AWS [Internet] KMA National Climate Data Center; 2022. [cited 2022 Nov 20]. Available from: https://data.kma.go.kr/data/grnd/selectAwsRltmList.do?pgmNo=56 . [Google Scholar]
- 7.Ree HI. Studies on Anopheles sinensis, the vector species of vivax malaria in Korea. Korean J Parasitol. 2005;43:75–92. doi: 10.3347/kjp.2005.43.3.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.KMA National Climate Data Center, author. Weather report [Internet] KMA National Climate Data Center; 2022. [cited 2023 Mar 10]. Available from: https://data.kma.go.kr/data/weatherReport/wsrList.do?pgmNo=647 . [Google Scholar]
- 9.Lee DK, Kim SJ. Seasonal prevalence of mosquitoes and weather factors influencing population size of Anopheles sinensis (Diptera, Culicidae) in Busan, Korea. Korean J Entomol. 2001;31:183–8. [Google Scholar]
- 10.Mordecai EA, Paaijmans KP, Johnson LR, et al. Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol Lett. 2013;16:22–30. doi: 10.1111/ele.12015. [DOI] [PubMed] [Google Scholar]
- 11.World Health Organization, author. World malaria report 2022. World Health Organization; 2022. [Google Scholar]
- 12.Kim HC, Kim MS, Choi KS, Hwang DU, Johnson JL, Klein TA. Comparison of adult mosquito black-light and light-emitting diode traps at three cowsheds located in malaria-endemic areas of the Republic of Korea. J Med Entomol. 2017;54:221–8. doi: 10.1093/jme/tjw136. [DOI] [PubMed] [Google Scholar]
