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Public Health Weekly Report 2023; 16(26): 852-866

Published online July 6, 2023

https://doi.org/10.56786/PHWR.2023.16.26.3

© The Korea Disease Control and Prevention Agency

Status of Malaria and Diagnosis Rate in the Republic of Korea, 2018-2022

HyunJung Kim, So-dam Lee, Na-Ri Shin, Kyungwon Hwang*

Division of Control for Zoonotic and Vecter borne Disease, Bureau of Infectious Disease Policy, Korea Disease Control and Prevention Agency, Cheongju, Korea

*Corresponding author: Kyungwon Hwang, Tel: +82-43-719-7160, E-mail: kirk99@korea.kr

Received: April 12, 2023; Revised: May 9, 2023; Accepted: May 10, 2023

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Malaria is a mosquito-borne disease designated as a Class-3 infectious disease in the Republic of Korea (ROK). Since the malaria outbreak in the military camps at Paju, an area near North Korea in 1993, the ROK has continuously witnessed the occurrence of malaria. As per the World Health Organization (WHO), the ROK is a malaria elimination target country, and the Korea Disease Control and Prevention Agency (KCDA) is promoting a five-year (2019–2023) action plan to eliminate malaria. Over the past five years, the number of malaria cases in the ROK have decreased slightly every year since 1998. However, the ROK remains far from malaria elimination, which aims at zero indigenous cases. The action plan aims to analyze the diagnosis rate within five days and initiates epidemiological investigation rate. Most of the malaria cases in the ROK occur mainly between April and October. By region, 59.2% of all cases occur in Gyeonggi-do, and Incheon had the highest incidence rate (2.1) per 100,000 people. Altogether, 64.4% of the total malaria cases have been reported from 30 districts that have been designated as malaria-risk areas. The indicators were found to be 73.6% in the diagnosis rate within five days and 81.7% in the epidemiological investigation rate. In the malaria-risk areas, the disease diagnosis and epidemiological investigations took a shorter time than in other regions. It was confirmed that the time of diagnosis after the onset of malaria symptoms was 4.75 days across the nation. In countries that have been certified by WHO for malaria elimination, rapid diagnosis and treatment are major strategies that have contributed to disease eradication. Thus, various approaches for prevention, diagnosis, and medium management are necessary to eliminate malaria.

Key words Vector Borne Diseases; Malaria; Early Diagnosis; Epidemiological investigation

Key messages

① What is known previously?

Since the re-appearance of malaria cases in the North Korean border in 1993, the Republic of Korea has been designated as a WHO malaria elimination target country. From that point on, the nation is promoting a five-year action plan to eliminate malaria.

② What new information is presented?

Patient diagnosis and epidemiological investigations in malaria-risk areas are being conducted in a short time compared to other regions. However, more active efforts are necessary to attain malaria elimination.

③ What are implications?

Rapid patient identification and management are the most important factors in malaria elimination. Thus, it is necessary to review the education process for rapid diagnosis and initiate publicity programs to improve malaria awareness.

Malaria is an acute febrile infectious disease caused by the protozoa Plasmodium (P. vivax, P. ovale, P. malariae, P. falciparum, P. knowlesi). In the Republic of Korea (ROK), it is designated as a Class-3 infectious disease and managed accordingly. Although the ROK received malaria elimination certification from the World Health Organization (WHO) in 1979, malaria cases have persisted, particularly in border areas with North Korea, since the initial outbreak among military personnel in Paju in 1993.

The Korea Disease Control and Prevention Agency (KDCA) has established a comprehensive and systematic “5-year Action Plan to Re-eradicate Malaria (2019–2023),” with a focus on key strategies for re-elimination of malaria, such as strengthening patient management, enhancing mosquito surveillance, and controlling vector mosquitoes. As of 2023, to accelerate re-elimination of malaria, the KDCA is expanding the list of areas targeted for malaria elimination from 20 areas (such as cities, counties, and districts) to 30 areas. In addition, areas adjacent to the high-risk areas are being classified as latent-risk areas, allowing for stronger control.

A total of 30 areas (i.e., cities, counties, and districts) in northern Incheon, Gyeonggi-do, and Gangwon-do are included as high-risk areas for malaria. Among the neighboring regions, 18 areas (including cities, counties, and districts) that have reported at least one case of malaria in the past 3 years are being designated as latent-risk areas (Table 1).

Table 1. 2023 Malaria risk area
ClassificationStateCountyTotal
Risk-areas(30 counties)IncheonGanghwa-gun, Gyeyang-gu, Namdong-gu, Dong-gu, Michuhol-gu, Bupyeong-gu, Seo-gu, Yeonsu-gu, Ongjin-gun, Jung-gu10
Gyeonggi-doGapyeong-gun, Goyang-si Deogyang-gu, Goyang-si Ilsandong-gu, Goyang-si Ilsanseo-gu, Guri-si, Gimpo-si, Namyangju-si, Dongducheon-si, Yangju-si, Yeoncheon-gun, Uijeongbu-si, Paju-si, Pocheon-si13
Gangwon-doGoseong-gun, Yanggu-gun, Inje-gun, Cheorwon-gun, Chuncheon-si, Hongcheon-gun, Hwacheon-gun7
Latent-risk areas(18 counties)SeoulGangseo-gu, Mapo-gu, Eunpyeong-gu, Jongno-gu, Seongbuk-gu, Gangbuk-gu, Dobong-gu, Nowon-gu, Jungnang-gu, Gwangjin-gu, Gangdong-gu11
Gyeonggi-doBucheon-si, Siheung-si, Hanam-si, Gwangju-si, Yangpyeong-gun5
Gangwon-doSokcho-si, Gangneung-si2

Values are presented as number only.



Based on analysis of reported cases and epidemiological investigations from 2018 to 2022 in both malaria control areas (high-risk areas and latent-risk areas) and other regions, the aim of this study was to assess the current status of patient management in malaria cases and explore control management approaches for malaria elimination.

1. Participants

We enrolled patients with malaria through the Integrated Disease Surveillance and Response system from January 1, 2018, to December 31, 2022, including patients diagnosed or suspected with malaria and pathogen carriers but excluding those with recurrent malaria. Over the 5-year period from 2018 to 2022, a total of 2,234 reported malaria cases were recorded, with an annual incidence of 400–500 cases, except for that in 2021 when there was a decrease in the number of cases due to the COVID-19 pandemic and the suspension of overseas travel and outdoor activities (Table 2). Based on reports of infectious disease from medical institutions and epidemiological surveys conducted by local public health centers, we differentiated between imported and domestic cases and included 1,998 domestic patients with malaria in the main analysis.

Table 2. Number of reported malaria cases in the Republic of Korea (2018–2022)
YearTotalJan.Feb.Mar.Apr.MayJun.Jul.Aug.Sep.Oct.Nov.Dec.
Total2,234242120791944785384122521563129
2018576763305912913792534677
20195596541038111154114643986
20203858769228711078351544
20212940252445596045331461
20224203126309277836742611


2. Survey Content and Methods

In this survey, we analyzed the occurrence status of reported cases by month and year based on the timing of case reports. Through case reports and epidemiological follow-up reports, we investigated various factors, such as the infection source (imported or domestic), civilian status (civilian, current military personnel, or ex-military personnel [discharged/retired in the past 2 years]), patient characteristics (e.g., sex, age, and place of residence), and time of infection and report (time of symptom onset, first hospital visit, diagnosis, report, and epidemiological follow-up).

In the 2023 malaria control guidelines, 30 high-risk and 18 latent-risk areas have been identified. We differentiated patients based on the control level of the area and analyzed patient management indices based on the time of symptom onset, diagnosis, report, and epidemiological follow-up for confirmed malaria cases.

As an outcome or performance indicator in the stage-1 malaria elimination plan, the 5-day diagnosis rate was calculated using the number of diagnosed cases within 5 days of symptom onset, as determined by epidemiological investigations. Asymptomatic patients were analyzed by treating the date of the first hospital visit as the date of symptom onset. Considering that the 2023 malaria control guidelines recommend performing an epidemiological follow-up within 3 days of case reporting, the rate of epidemiological follow-up was calculated using the number of epidemiological investigations conducted within 3 days of the date of case reporting, excluding weekends.

To compare patient monitoring and management among high-risk, latent-risk, and undesignated areas, we also analyzed the “days until diagnosis” and “days until epidemiological follow-up.” Days until diagnosis was defined as the number of days from the date of symptom onset to the date of diagnosis, and days until epidemiological follow-up was defined as the number of days from the date of case reporting to the date of epidemiological follow-up. Unlike that for the epidemiological follow-up rate analysis, we did not exclude weekends in this analysis. Analysis of variance (ANOVA) was used to investigate between-group differences among high-risk, latent-risk, and undesignated areas, using Scheffé’s test for the post-hoc analysis. All statistical analyses were performed using SPSS 22.0 (SPSS Inc.).

1. Malaria Cases in the Republic of Korea (2018–2022)

A total of 2,234 malaria cases have been reported in the past 5 years (2018–2022) in the ROK, with 576 cases reported in 2018, 559 cases in 2019, 385 cases in 2020, 294 cases in 2021, and 420 cases in 2022, suggesting that the number of cases has been slowly decreasing. Of these, 2,109 (94.4%) cases were reported from April to October (Table 2).

Among all reported cases, 1,998 (89.4%) were domestically acquired. Ex-military and current military personnel accounted for 235 and 300 cases, respectively, representing 26.8% of the total cases. Even after excluding current and ex-military cases (535 people), men (1,130 people) accounted for approximately 3.4 times more cases than women (333 people), and patients aged 20–59 years accounted for 81.4% of all cases (Table 3).

Table 3. General characteristics of malaria cases (2018–2022)
CharacteristicTotal20182019202020212022
No.%
Total1,998100.0501485356274382
Sex
Male1,665 (535)83.3441 (163)389 (121)297 (83)213 (62)325 (106)
Female33316.76096596157
Age (yr)
0–923 (0)1.246454
10–1910 2(9)5.131 (1)22 (2)1610 (1)23 (5)
20–29707 (499)35.4207 (154)155 (113)112 (78)97 (61)136 (93)
30–39283 (15)14.263 (3)71 (2)52 (4)36 (0)61 (2)
40–49315 (10)15.872 (4)82 (3)63 (1)40 (0)58 (2)
50–59319 (2)16.074 (1)69 (1)63 (0)46 (0)67 (0)
60–69164 (0)8.23746263223
70–7965 (0)3.312271457
80–8918 (0)0.915633
90–992 (0)0.102000

Values are presented as number (soldiers).



Analyzing the occurrence status by area, we found 1,182 (59.2%) cases in Gyeonggi-do, 310 (15.5%) cases in Incheon, and 268 (13.4%) cases in Seoul. After adjusting these figures for population size, 2.1 cases/100,000 population were reported in Incheon, 1.8 cases/100,000 population in Gyeonggi-do, and 0.6 cases/100,000 population in Seoul (Table 4).

Table 4. Incidence rates of malaria by region (2018–2022)
YearTotal20182019202020212022
No.Ratea)No.Ratea)No.Ratea)No.Ratea)No.Ratea)No.Ratea)
Total1,9980.85011.04850.93560.72740.53820.7
Seoul2680.6610.6720.7480.5350.4520.6
Busan260.260.2100.310.020.170.2
Deagu190.2120.520.120.110.020.1
Incheon3102.1742.5842.8471.6451.5602.0
Geangju70.120.140.310.100.000.0
Daejeon190.330.240.330.220.170.5
Ulsan100.210.110.130.320.230.3
Sejong20.110.300.010.300.000.0
Gyeonggi-do1,1821.83022.32702.02181.61681.22241.6
Gangwon-do540.790.6151.0100.680.5120.8
Chungbuk170.220.140.250.330.230.2
Chungnam230.240.270.360.330.130.1
Jeonbuk120.130.220.140.200.030.2
Jeonnam110.150.300.010.120.130.2
Gyeongbuk110.120.140.220.120.110.0
Gyeongnam220.1120.440.140.110.010.0
Jeju50.120.320.300.000.010.1

a)Incidence rate per million.



2. Current State of Malaria Management in the Republic of Korea

Of the total malaria cases in the ROK, 1,297 (64.9%) cases were reported in high-risk areas. The incidence was 3.5 cases/100,00 population in high-risk areas, 0.7 cases/100,000 population in latent-risk areas, and 0.3 cases/100,000 population in undesignated areas (Table 5).

Table 5. Status of malaria cases management in the Republic of Korea
ClassificationNationRisk-areas (30 counties)Latent-risk areas (18 counties)Other areas (202 counties)
Cases
No.1,998 (100)1,297 (64.9)222 (11.1)479 (24.0)
Ratea)0.83.50.70.3
Indicaters
Diagnosis within 5 days68.773.664.457.4
Investigation within 3 days78.081.774.375.4

Values are presented as number (%). a)Incidence rate per million.



The 5-day diagnosis rate, which was considered as outcome or performance indicator in the stage-1 malaria elimination plan, was 73.6% in high-risk areas, 64.4% in latent-risk areas, and 57.4% in undesignated areas. The 3-day epidemiological follow-up rate was 81.7% in high-risk areas, 74.3% in latent-risk areas, and 75.4% in undesignated areas.

The number of days until diagnosis was significantly fewer in high-risk areas (mean, 4.0 days; F = 5.772; p<0.05) than in latent-risk (mean, 6.7 days) and undesignated (mean, 5.8 days) areas, and the number of days until epidemiological follow-up was also significantly fewer in high-risk areas (mean, 6.2 days; F = 13.153; p<0.001) than in latent-risk (mean, 15.1 days) and undesignated (mean, 13.0 days; Tables 5, 6) areas. Scheffé’s test confirmed that the number of days until diagnosis and until epidemiological follow-up was significantly fewer in high-risk areas than in low-risk and undesignated areas but did not differ significantly between latent-risk and undesignated areas.

Table 6. Time of malaria diagnosis and epidemiologic investigation
CategoryNation
(n=1,998)
Risk-areasa
(n=1,297)
Latent-risk areasb (n=222)Other areasc
(n=479)
Fp-valueScheffé’s test
Diagnosis time4.6±13.04.0±11.36.7±25.85.8±7.45.772p<0.05a
Investigation time8.9±31.06.2±22.515.1±48.113.0±38.713.153p<0.001a

Values are presented as mean±standard deviation.


Domestic cases of malaria have been persistently reported in the ROK since its re-emergence in 1993. In the past 5 years, approximately 400–500 cases of malaria have been confirmed annually, indicating that we are still far from the goal of zero domestic malaria cases by 2030, as outlined in the malaria elimination plan.

Since malaria is transmitted through mosquito bites from infected vectors, its prevalence can be affected by various factors such as climate change that promotes mosquito population growth, the behavior of mosquito vectors, and the behavioral characteristics of the population. As observed in the distribution of malaria cases over the past 5 years, men (83.3%) accounted for significantly more number of cases than women (81.4%) among individuals aged 20–59 years. Analyzing the pattern of confirmed cases by sex and age, a large proportion of confirmed malaria cases are reported in adult men, which could be explained by social behavioral characteristics of adult men, considering that men are more likely to be active at night, which is the feeding time of malaria vector mosquitoes.

The incidence of domestic malaria cases in the ROK was 0.8 cases/100,000 population. By area, the incidence was the highest in Incheon (2.1 cases/100,000 population), followed by that in Gyeonggi-do (1.8 cases/100,000 population) and Seoul (0.6 cases/100,000 population), showing that cases are mostly occurring in regions bordering the DPRK. The KDCA is currently conducting a nationally funded project to designate high-risk areas where malaria occurs frequently and to improve malaria control in these areas. Among the regions with high malaria incidence, 30 areas (cities, counties, and districts) have been selected as high-risk areas.

To prevent the transmission of malaria, the KDCA recommends that the diagnosis and treatment should start within 5 days of symptom onset. In high-risk areas, the average number of days within which the diagnosis is made is 4 days, and the diagnosis is made within an average of 5 days in 73.6% of cases. In latent-risk and undesignated areas, the mean time to diagnosis exceeded the 5-day recommendation, at 6.7 and 5.8 days, respectively, whereas the number of cases diagnosed within 5 days was 64.4% in latent-risk areas and 57.4% in undesignated areas. In high-risk areas, healthcare professionals have more experience in dealing with malaria cases, and local residents have high awareness of the disease, leading to prompt diagnosis and reporting. However, the 5-day diagnosis rate remains below 80%, and the nationwide average rate is as low as 68.7%. Although the diagnosis was made faster in high-risk areas, which are the target areas of a nationally funded project, reviewing the 5-day diagnosis rate as a patient management index is important, considering that the incidence of malaria remains high.

An epidemiological follow-up within 3 days of case reporting is recommended for malaria as well as most legally designated infectious diseases. In the epidemiological follow-up for malaria, identifying the route of infection and investigating the surrounding environment are important to prevent further spread. The mean days until epidemiological follow-up in high-risk areas during the past 5 years was 6.2 days, which exceeds the 3-day recommendation; epidemiological follow-up was achieved within 3 days in 81.7% of cases. The mean days until epidemiological follow-up in latent-risk and undesignated areas were 15.1 and 13.0 days, respectively, while the 3-day epidemiological follow-up rates were 74.3% and 75.4%, respectively, implying delayed epidemiological follow-up in these regions compared with that in high-risk areas. The potential causes of delayed epidemiological follow-up include the frequent turnover of infectious disease local government officials and lack of interest from local authorities because of the low incidence and high mortality of malaria.

Considering the examples of other countries certified by the WHO as malaria-free, China introduced their “1-3-7 strategy” as key to successful malaria elimination. In this strategy, malaria should be reported within 1 day, and epidemiological follow-up should performed within 3 days. Furthermore, efforts should be made to prevent further spread within 7 days.

Based on the findings of this study, it is evident that the early patient detection and case management strategies employed in the ROK have been ineffective in reducing the incidence of malaria in the past 5 years. As shown by the WHO malaria elimination guidelines, including the case of China, a multidimensional approach is required for malaria elimination, encompassing monitoring and management of patients and prevention, diagnosis, treatment, and vector control of malaria. Moreover, seamless information exchange and feedback between healthcare facilities, local authorities, and the KDCA are essential.

To accelerate re-elimination of malaria, the KDCA aims to pursue the stage-2 Action Plan to Re-eradicate Malaria (2024–2028). The strategy in stage 2 will be based on efficient monitoring and responses in the active foci of malaria (i.e., areas with high malaria incidence) through rapid diagnosis, complete treatment guarantee, focused management and response for each patient, improved monitoring based on case studies, efficient elimination of disease vectors, and disease prevention.

Ethics Statement: Not applicable.

Funding Source: None.

Acknowledgments: None.

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

Author Contributions: Conceptualization: HJK, SL, NRS, KH. Data curation: HJK, SL. Formal analysis: HJK. Investigation: SL. Methodology: HJK, NRS, KH. Project administration: NRS. Resources: HJK. Supervision: NRS, KH. Visualization: HJK. Writing – original draft: HJK. Writing – review & editing: NRS, KH.

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  2. WHO. Preparing for certification of malaria elimination. WHO 2022; 2nd ed.
  3. WHO. A framework for malaria elimination. WHO; 2017.
  4. Park JW. Status of Plasmodium vivax malaria in the Republic of Korea after reemergence. Hanyang Med Rev 2010;30:176-86.
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  5. WHO. Zeroing in on malaria elimination: final report of the E-2020 initiative. WHO; 2021.
  6. Feng X, Huang F, Yin J, Wang R, Xia Z. Key takeaways from China's success in eliminating malaria: leveraging existing evidence for a malaria-free world. BMJ Glob Health 2022;7:e008351.
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  7. Bahk YY, Lee HW, Na BK, et al. Epidemiological characteristics of re-emerging vivax malaria in the Republic of Korea (1993-2017). Korean J Parasitol 2018;56:531-43.
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Surveillance Reports

Public Health Weekly Report 2023; 16(26): 852-866

Published online July 6, 2023 https://doi.org/10.56786/PHWR.2023.16.26.3

Copyright © The Korea Disease Control and Prevention Agency.

Status of Malaria and Diagnosis Rate in the Republic of Korea, 2018-2022

HyunJung Kim, So-dam Lee, Na-Ri Shin, Kyungwon Hwang*

Division of Control for Zoonotic and Vecter borne Disease, Bureau of Infectious Disease Policy, Korea Disease Control and Prevention Agency, Cheongju, Korea

Correspondence to:*Corresponding author: Kyungwon Hwang, Tel: +82-43-719-7160, E-mail: kirk99@korea.kr

Received: April 12, 2023; Revised: May 9, 2023; Accepted: May 10, 2023

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Malaria is a mosquito-borne disease designated as a Class-3 infectious disease in the Republic of Korea (ROK). Since the malaria outbreak in the military camps at Paju, an area near North Korea in 1993, the ROK has continuously witnessed the occurrence of malaria. As per the World Health Organization (WHO), the ROK is a malaria elimination target country, and the Korea Disease Control and Prevention Agency (KCDA) is promoting a five-year (2019–2023) action plan to eliminate malaria. Over the past five years, the number of malaria cases in the ROK have decreased slightly every year since 1998. However, the ROK remains far from malaria elimination, which aims at zero indigenous cases. The action plan aims to analyze the diagnosis rate within five days and initiates epidemiological investigation rate. Most of the malaria cases in the ROK occur mainly between April and October. By region, 59.2% of all cases occur in Gyeonggi-do, and Incheon had the highest incidence rate (2.1) per 100,000 people. Altogether, 64.4% of the total malaria cases have been reported from 30 districts that have been designated as malaria-risk areas. The indicators were found to be 73.6% in the diagnosis rate within five days and 81.7% in the epidemiological investigation rate. In the malaria-risk areas, the disease diagnosis and epidemiological investigations took a shorter time than in other regions. It was confirmed that the time of diagnosis after the onset of malaria symptoms was 4.75 days across the nation. In countries that have been certified by WHO for malaria elimination, rapid diagnosis and treatment are major strategies that have contributed to disease eradication. Thus, various approaches for prevention, diagnosis, and medium management are necessary to eliminate malaria.

Keywords: Vector Borne Diseases, Malaria, Early Diagnosis, Epidemiological investigation

Body

Key messages

① What is known previously?

Since the re-appearance of malaria cases in the North Korean border in 1993, the Republic of Korea has been designated as a WHO malaria elimination target country. From that point on, the nation is promoting a five-year action plan to eliminate malaria.

② What new information is presented?

Patient diagnosis and epidemiological investigations in malaria-risk areas are being conducted in a short time compared to other regions. However, more active efforts are necessary to attain malaria elimination.

③ What are implications?

Rapid patient identification and management are the most important factors in malaria elimination. Thus, it is necessary to review the education process for rapid diagnosis and initiate publicity programs to improve malaria awareness.

Introduction

Malaria is an acute febrile infectious disease caused by the protozoa Plasmodium (P. vivax, P. ovale, P. malariae, P. falciparum, P. knowlesi). In the Republic of Korea (ROK), it is designated as a Class-3 infectious disease and managed accordingly. Although the ROK received malaria elimination certification from the World Health Organization (WHO) in 1979, malaria cases have persisted, particularly in border areas with North Korea, since the initial outbreak among military personnel in Paju in 1993.

The Korea Disease Control and Prevention Agency (KDCA) has established a comprehensive and systematic “5-year Action Plan to Re-eradicate Malaria (2019–2023),” with a focus on key strategies for re-elimination of malaria, such as strengthening patient management, enhancing mosquito surveillance, and controlling vector mosquitoes. As of 2023, to accelerate re-elimination of malaria, the KDCA is expanding the list of areas targeted for malaria elimination from 20 areas (such as cities, counties, and districts) to 30 areas. In addition, areas adjacent to the high-risk areas are being classified as latent-risk areas, allowing for stronger control.

A total of 30 areas (i.e., cities, counties, and districts) in northern Incheon, Gyeonggi-do, and Gangwon-do are included as high-risk areas for malaria. Among the neighboring regions, 18 areas (including cities, counties, and districts) that have reported at least one case of malaria in the past 3 years are being designated as latent-risk areas (Table 1).

2023 Malaria risk area
ClassificationStateCountyTotal
Risk-areas(30 counties)IncheonGanghwa-gun, Gyeyang-gu, Namdong-gu, Dong-gu, Michuhol-gu, Bupyeong-gu, Seo-gu, Yeonsu-gu, Ongjin-gun, Jung-gu10
Gyeonggi-doGapyeong-gun, Goyang-si Deogyang-gu, Goyang-si Ilsandong-gu, Goyang-si Ilsanseo-gu, Guri-si, Gimpo-si, Namyangju-si, Dongducheon-si, Yangju-si, Yeoncheon-gun, Uijeongbu-si, Paju-si, Pocheon-si13
Gangwon-doGoseong-gun, Yanggu-gun, Inje-gun, Cheorwon-gun, Chuncheon-si, Hongcheon-gun, Hwacheon-gun7
Latent-risk areas(18 counties)SeoulGangseo-gu, Mapo-gu, Eunpyeong-gu, Jongno-gu, Seongbuk-gu, Gangbuk-gu, Dobong-gu, Nowon-gu, Jungnang-gu, Gwangjin-gu, Gangdong-gu11
Gyeonggi-doBucheon-si, Siheung-si, Hanam-si, Gwangju-si, Yangpyeong-gun5
Gangwon-doSokcho-si, Gangneung-si2

Values are presented as number only..



Based on analysis of reported cases and epidemiological investigations from 2018 to 2022 in both malaria control areas (high-risk areas and latent-risk areas) and other regions, the aim of this study was to assess the current status of patient management in malaria cases and explore control management approaches for malaria elimination.

Methods

1. Participants

We enrolled patients with malaria through the Integrated Disease Surveillance and Response system from January 1, 2018, to December 31, 2022, including patients diagnosed or suspected with malaria and pathogen carriers but excluding those with recurrent malaria. Over the 5-year period from 2018 to 2022, a total of 2,234 reported malaria cases were recorded, with an annual incidence of 400–500 cases, except for that in 2021 when there was a decrease in the number of cases due to the COVID-19 pandemic and the suspension of overseas travel and outdoor activities (Table 2). Based on reports of infectious disease from medical institutions and epidemiological surveys conducted by local public health centers, we differentiated between imported and domestic cases and included 1,998 domestic patients with malaria in the main analysis.

Number of reported malaria cases in the Republic of Korea (2018–2022)
YearTotalJan.Feb.Mar.Apr.MayJun.Jul.Aug.Sep.Oct.Nov.Dec.
Total2,234242120791944785384122521563129
2018576763305912913792534677
20195596541038111154114643986
20203858769228711078351544
20212940252445596045331461
20224203126309277836742611


2. Survey Content and Methods

In this survey, we analyzed the occurrence status of reported cases by month and year based on the timing of case reports. Through case reports and epidemiological follow-up reports, we investigated various factors, such as the infection source (imported or domestic), civilian status (civilian, current military personnel, or ex-military personnel [discharged/retired in the past 2 years]), patient characteristics (e.g., sex, age, and place of residence), and time of infection and report (time of symptom onset, first hospital visit, diagnosis, report, and epidemiological follow-up).

In the 2023 malaria control guidelines, 30 high-risk and 18 latent-risk areas have been identified. We differentiated patients based on the control level of the area and analyzed patient management indices based on the time of symptom onset, diagnosis, report, and epidemiological follow-up for confirmed malaria cases.

As an outcome or performance indicator in the stage-1 malaria elimination plan, the 5-day diagnosis rate was calculated using the number of diagnosed cases within 5 days of symptom onset, as determined by epidemiological investigations. Asymptomatic patients were analyzed by treating the date of the first hospital visit as the date of symptom onset. Considering that the 2023 malaria control guidelines recommend performing an epidemiological follow-up within 3 days of case reporting, the rate of epidemiological follow-up was calculated using the number of epidemiological investigations conducted within 3 days of the date of case reporting, excluding weekends.

To compare patient monitoring and management among high-risk, latent-risk, and undesignated areas, we also analyzed the “days until diagnosis” and “days until epidemiological follow-up.” Days until diagnosis was defined as the number of days from the date of symptom onset to the date of diagnosis, and days until epidemiological follow-up was defined as the number of days from the date of case reporting to the date of epidemiological follow-up. Unlike that for the epidemiological follow-up rate analysis, we did not exclude weekends in this analysis. Analysis of variance (ANOVA) was used to investigate between-group differences among high-risk, latent-risk, and undesignated areas, using Scheffé’s test for the post-hoc analysis. All statistical analyses were performed using SPSS 22.0 (SPSS Inc.).

Results

1. Malaria Cases in the Republic of Korea (2018–2022)

A total of 2,234 malaria cases have been reported in the past 5 years (2018–2022) in the ROK, with 576 cases reported in 2018, 559 cases in 2019, 385 cases in 2020, 294 cases in 2021, and 420 cases in 2022, suggesting that the number of cases has been slowly decreasing. Of these, 2,109 (94.4%) cases were reported from April to October (Table 2).

Among all reported cases, 1,998 (89.4%) were domestically acquired. Ex-military and current military personnel accounted for 235 and 300 cases, respectively, representing 26.8% of the total cases. Even after excluding current and ex-military cases (535 people), men (1,130 people) accounted for approximately 3.4 times more cases than women (333 people), and patients aged 20–59 years accounted for 81.4% of all cases (Table 3).

General characteristics of malaria cases (2018–2022)
CharacteristicTotal20182019202020212022
No.%
Total1,998100.0501485356274382
Sex
Male1,665 (535)83.3441 (163)389 (121)297 (83)213 (62)325 (106)
Female33316.76096596157
Age (yr)
0–923 (0)1.246454
10–1910 2(9)5.131 (1)22 (2)1610 (1)23 (5)
20–29707 (499)35.4207 (154)155 (113)112 (78)97 (61)136 (93)
30–39283 (15)14.263 (3)71 (2)52 (4)36 (0)61 (2)
40–49315 (10)15.872 (4)82 (3)63 (1)40 (0)58 (2)
50–59319 (2)16.074 (1)69 (1)63 (0)46 (0)67 (0)
60–69164 (0)8.23746263223
70–7965 (0)3.312271457
80–8918 (0)0.915633
90–992 (0)0.102000

Values are presented as number (soldiers)..



Analyzing the occurrence status by area, we found 1,182 (59.2%) cases in Gyeonggi-do, 310 (15.5%) cases in Incheon, and 268 (13.4%) cases in Seoul. After adjusting these figures for population size, 2.1 cases/100,000 population were reported in Incheon, 1.8 cases/100,000 population in Gyeonggi-do, and 0.6 cases/100,000 population in Seoul (Table 4).

Incidence rates of malaria by region (2018–2022)
YearTotal20182019202020212022
No.Ratea)No.Ratea)No.Ratea)No.Ratea)No.Ratea)No.Ratea)
Total1,9980.85011.04850.93560.72740.53820.7
Seoul2680.6610.6720.7480.5350.4520.6
Busan260.260.2100.310.020.170.2
Deagu190.2120.520.120.110.020.1
Incheon3102.1742.5842.8471.6451.5602.0
Geangju70.120.140.310.100.000.0
Daejeon190.330.240.330.220.170.5
Ulsan100.210.110.130.320.230.3
Sejong20.110.300.010.300.000.0
Gyeonggi-do1,1821.83022.32702.02181.61681.22241.6
Gangwon-do540.790.6151.0100.680.5120.8
Chungbuk170.220.140.250.330.230.2
Chungnam230.240.270.360.330.130.1
Jeonbuk120.130.220.140.200.030.2
Jeonnam110.150.300.010.120.130.2
Gyeongbuk110.120.140.220.120.110.0
Gyeongnam220.1120.440.140.110.010.0
Jeju50.120.320.300.000.010.1

a)Incidence rate per million..



2. Current State of Malaria Management in the Republic of Korea

Of the total malaria cases in the ROK, 1,297 (64.9%) cases were reported in high-risk areas. The incidence was 3.5 cases/100,00 population in high-risk areas, 0.7 cases/100,000 population in latent-risk areas, and 0.3 cases/100,000 population in undesignated areas (Table 5).

Status of malaria cases management in the Republic of Korea
ClassificationNationRisk-areas (30 counties)Latent-risk areas (18 counties)Other areas (202 counties)
Cases
No.1,998 (100)1,297 (64.9)222 (11.1)479 (24.0)
Ratea)0.83.50.70.3
Indicaters
Diagnosis within 5 days68.773.664.457.4
Investigation within 3 days78.081.774.375.4

Values are presented as number (%). a)Incidence rate per million..



The 5-day diagnosis rate, which was considered as outcome or performance indicator in the stage-1 malaria elimination plan, was 73.6% in high-risk areas, 64.4% in latent-risk areas, and 57.4% in undesignated areas. The 3-day epidemiological follow-up rate was 81.7% in high-risk areas, 74.3% in latent-risk areas, and 75.4% in undesignated areas.

The number of days until diagnosis was significantly fewer in high-risk areas (mean, 4.0 days; F = 5.772; p<0.05) than in latent-risk (mean, 6.7 days) and undesignated (mean, 5.8 days) areas, and the number of days until epidemiological follow-up was also significantly fewer in high-risk areas (mean, 6.2 days; F = 13.153; p<0.001) than in latent-risk (mean, 15.1 days) and undesignated (mean, 13.0 days; Tables 5, 6) areas. Scheffé’s test confirmed that the number of days until diagnosis and until epidemiological follow-up was significantly fewer in high-risk areas than in low-risk and undesignated areas but did not differ significantly between latent-risk and undesignated areas.

Time of malaria diagnosis and epidemiologic investigation
CategoryNation
(n=1,998)
Risk-areasa
(n=1,297)
Latent-risk areasb (n=222)Other areasc
(n=479)
Fp-valueScheffé’s test
Diagnosis time4.6±13.04.0±11.36.7±25.85.8±7.45.772p<0.05a
Investigation time8.9±31.06.2±22.515.1±48.113.0±38.713.153p<0.001a

Values are presented as mean±standard deviation..


Conclusions

Domestic cases of malaria have been persistently reported in the ROK since its re-emergence in 1993. In the past 5 years, approximately 400–500 cases of malaria have been confirmed annually, indicating that we are still far from the goal of zero domestic malaria cases by 2030, as outlined in the malaria elimination plan.

Since malaria is transmitted through mosquito bites from infected vectors, its prevalence can be affected by various factors such as climate change that promotes mosquito population growth, the behavior of mosquito vectors, and the behavioral characteristics of the population. As observed in the distribution of malaria cases over the past 5 years, men (83.3%) accounted for significantly more number of cases than women (81.4%) among individuals aged 20–59 years. Analyzing the pattern of confirmed cases by sex and age, a large proportion of confirmed malaria cases are reported in adult men, which could be explained by social behavioral characteristics of adult men, considering that men are more likely to be active at night, which is the feeding time of malaria vector mosquitoes.

The incidence of domestic malaria cases in the ROK was 0.8 cases/100,000 population. By area, the incidence was the highest in Incheon (2.1 cases/100,000 population), followed by that in Gyeonggi-do (1.8 cases/100,000 population) and Seoul (0.6 cases/100,000 population), showing that cases are mostly occurring in regions bordering the DPRK. The KDCA is currently conducting a nationally funded project to designate high-risk areas where malaria occurs frequently and to improve malaria control in these areas. Among the regions with high malaria incidence, 30 areas (cities, counties, and districts) have been selected as high-risk areas.

To prevent the transmission of malaria, the KDCA recommends that the diagnosis and treatment should start within 5 days of symptom onset. In high-risk areas, the average number of days within which the diagnosis is made is 4 days, and the diagnosis is made within an average of 5 days in 73.6% of cases. In latent-risk and undesignated areas, the mean time to diagnosis exceeded the 5-day recommendation, at 6.7 and 5.8 days, respectively, whereas the number of cases diagnosed within 5 days was 64.4% in latent-risk areas and 57.4% in undesignated areas. In high-risk areas, healthcare professionals have more experience in dealing with malaria cases, and local residents have high awareness of the disease, leading to prompt diagnosis and reporting. However, the 5-day diagnosis rate remains below 80%, and the nationwide average rate is as low as 68.7%. Although the diagnosis was made faster in high-risk areas, which are the target areas of a nationally funded project, reviewing the 5-day diagnosis rate as a patient management index is important, considering that the incidence of malaria remains high.

An epidemiological follow-up within 3 days of case reporting is recommended for malaria as well as most legally designated infectious diseases. In the epidemiological follow-up for malaria, identifying the route of infection and investigating the surrounding environment are important to prevent further spread. The mean days until epidemiological follow-up in high-risk areas during the past 5 years was 6.2 days, which exceeds the 3-day recommendation; epidemiological follow-up was achieved within 3 days in 81.7% of cases. The mean days until epidemiological follow-up in latent-risk and undesignated areas were 15.1 and 13.0 days, respectively, while the 3-day epidemiological follow-up rates were 74.3% and 75.4%, respectively, implying delayed epidemiological follow-up in these regions compared with that in high-risk areas. The potential causes of delayed epidemiological follow-up include the frequent turnover of infectious disease local government officials and lack of interest from local authorities because of the low incidence and high mortality of malaria.

Considering the examples of other countries certified by the WHO as malaria-free, China introduced their “1-3-7 strategy” as key to successful malaria elimination. In this strategy, malaria should be reported within 1 day, and epidemiological follow-up should performed within 3 days. Furthermore, efforts should be made to prevent further spread within 7 days.

Based on the findings of this study, it is evident that the early patient detection and case management strategies employed in the ROK have been ineffective in reducing the incidence of malaria in the past 5 years. As shown by the WHO malaria elimination guidelines, including the case of China, a multidimensional approach is required for malaria elimination, encompassing monitoring and management of patients and prevention, diagnosis, treatment, and vector control of malaria. Moreover, seamless information exchange and feedback between healthcare facilities, local authorities, and the KDCA are essential.

To accelerate re-elimination of malaria, the KDCA aims to pursue the stage-2 Action Plan to Re-eradicate Malaria (2024–2028). The strategy in stage 2 will be based on efficient monitoring and responses in the active foci of malaria (i.e., areas with high malaria incidence) through rapid diagnosis, complete treatment guarantee, focused management and response for each patient, improved monitoring based on case studies, efficient elimination of disease vectors, and disease prevention.

Declarations

Ethics Statement: Not applicable.

Funding Source: None.

Acknowledgments: None.

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

Author Contributions: Conceptualization: HJK, SL, NRS, KH. Data curation: HJK, SL. Formal analysis: HJK. Investigation: SL. Methodology: HJK, NRS, KH. Project administration: NRS. Resources: HJK. Supervision: NRS, KH. Visualization: HJK. Writing – original draft: HJK. Writing – review & editing: NRS, KH.

2023 Malaria risk area
ClassificationStateCountyTotal
Risk-areas(30 counties)IncheonGanghwa-gun, Gyeyang-gu, Namdong-gu, Dong-gu, Michuhol-gu, Bupyeong-gu, Seo-gu, Yeonsu-gu, Ongjin-gun, Jung-gu10
Gyeonggi-doGapyeong-gun, Goyang-si Deogyang-gu, Goyang-si Ilsandong-gu, Goyang-si Ilsanseo-gu, Guri-si, Gimpo-si, Namyangju-si, Dongducheon-si, Yangju-si, Yeoncheon-gun, Uijeongbu-si, Paju-si, Pocheon-si13
Gangwon-doGoseong-gun, Yanggu-gun, Inje-gun, Cheorwon-gun, Chuncheon-si, Hongcheon-gun, Hwacheon-gun7
Latent-risk areas(18 counties)SeoulGangseo-gu, Mapo-gu, Eunpyeong-gu, Jongno-gu, Seongbuk-gu, Gangbuk-gu, Dobong-gu, Nowon-gu, Jungnang-gu, Gwangjin-gu, Gangdong-gu11
Gyeonggi-doBucheon-si, Siheung-si, Hanam-si, Gwangju-si, Yangpyeong-gun5
Gangwon-doSokcho-si, Gangneung-si2

Values are presented as number only..


Number of reported malaria cases in the Republic of Korea (2018–2022)
YearTotalJan.Feb.Mar.Apr.MayJun.Jul.Aug.Sep.Oct.Nov.Dec.
Total2,234242120791944785384122521563129
2018576763305912913792534677
20195596541038111154114643986
20203858769228711078351544
20212940252445596045331461
20224203126309277836742611

General characteristics of malaria cases (2018–2022)
CharacteristicTotal20182019202020212022
No.%
Total1,998100.0501485356274382
Sex
Male1,665 (535)83.3441 (163)389 (121)297 (83)213 (62)325 (106)
Female33316.76096596157
Age (yr)
0–923 (0)1.246454
10–1910 2(9)5.131 (1)22 (2)1610 (1)23 (5)
20–29707 (499)35.4207 (154)155 (113)112 (78)97 (61)136 (93)
30–39283 (15)14.263 (3)71 (2)52 (4)36 (0)61 (2)
40–49315 (10)15.872 (4)82 (3)63 (1)40 (0)58 (2)
50–59319 (2)16.074 (1)69 (1)63 (0)46 (0)67 (0)
60–69164 (0)8.23746263223
70–7965 (0)3.312271457
80–8918 (0)0.915633
90–992 (0)0.102000

Values are presented as number (soldiers)..


Incidence rates of malaria by region (2018–2022)
YearTotal20182019202020212022
No.Ratea)No.Ratea)No.Ratea)No.Ratea)No.Ratea)No.Ratea)
Total1,9980.85011.04850.93560.72740.53820.7
Seoul2680.6610.6720.7480.5350.4520.6
Busan260.260.2100.310.020.170.2
Deagu190.2120.520.120.110.020.1
Incheon3102.1742.5842.8471.6451.5602.0
Geangju70.120.140.310.100.000.0
Daejeon190.330.240.330.220.170.5
Ulsan100.210.110.130.320.230.3
Sejong20.110.300.010.300.000.0
Gyeonggi-do1,1821.83022.32702.02181.61681.22241.6
Gangwon-do540.790.6151.0100.680.5120.8
Chungbuk170.220.140.250.330.230.2
Chungnam230.240.270.360.330.130.1
Jeonbuk120.130.220.140.200.030.2
Jeonnam110.150.300.010.120.130.2
Gyeongbuk110.120.140.220.120.110.0
Gyeongnam220.1120.440.140.110.010.0
Jeju50.120.320.300.000.010.1

a)Incidence rate per million..


Status of malaria cases management in the Republic of Korea
ClassificationNationRisk-areas (30 counties)Latent-risk areas (18 counties)Other areas (202 counties)
Cases
No.1,998 (100)1,297 (64.9)222 (11.1)479 (24.0)
Ratea)0.83.50.70.3
Indicaters
Diagnosis within 5 days68.773.664.457.4
Investigation within 3 days78.081.774.375.4

Values are presented as number (%). a)Incidence rate per million..


Time of malaria diagnosis and epidemiologic investigation
CategoryNation
(n=1,998)
Risk-areasa
(n=1,297)
Latent-risk areasb (n=222)Other areasc
(n=479)
Fp-valueScheffé’s test
Diagnosis time4.6±13.04.0±11.36.7±25.85.8±7.45.772p<0.05a
Investigation time8.9±31.06.2±22.515.1±48.113.0±38.713.153p<0.001a

Values are presented as mean±standard deviation..


References

  1. Korea Disease Control and Prevention Agency. Malaria control guideline. Korea Disease Control and Prevention Agency; 2023.
  2. WHO. Preparing for certification of malaria elimination. WHO 2022; 2nd ed.
  3. WHO. A framework for malaria elimination. WHO; 2017.
  4. Park JW. Status of Plasmodium vivax malaria in the Republic of Korea after reemergence. Hanyang Med Rev 2010;30:176-86.
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  5. WHO. Zeroing in on malaria elimination: final report of the E-2020 initiative. WHO; 2021.
  6. Feng X, Huang F, Yin J, Wang R, Xia Z. Key takeaways from China's success in eliminating malaria: leveraging existing evidence for a malaria-free world. BMJ Glob Health 2022;7:e008351.
    Pubmed KoreaMed CrossRef
  7. Bahk YY, Lee HW, Na BK, et al. Epidemiological characteristics of re-emerging vivax malaria in the Republic of Korea (1993-2017). Korean J Parasitol 2018;56:531-43.
    Pubmed KoreaMed CrossRef

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