Abstract
Lyme disease is an infectious illness that is transmitted by the bite of a tick infected with the pathogen Borrelia burgdorferi. In the Republic of Korea, the pathogen was isolated from ticks in the early 1990s and has been designated and managed as a statutory infectious disease since 2010. This study analyzed the epidemiological investigation data of 116 patients with Lyme disease reported to the Disease and Health Integrated Management System (https://is.kdca.go.kr/) from 2019 to 2023 to determine the recent outbreak pattern of Lyme disease. We aimed to determine the epidemiological characteristics. The number of patients with Lyme disease decreased during the COVID-19 pandemic but increased approximately six-fold in 2023 compared with 2021. Most cases of domestic infection (72.4%) occurred between June and November, and were related to various outdoor activities, such as one-time outdoor activities (42.1%) and farm and garden work (40.4%) in summer and fall (72.4%). Lyme disease presents a low fatality rate; however, if it does not receive appropriate treatment in the early stages, it becomes chronic. Therefore, it is important to reduce exposure to ticks to prevent individuals from being bitten during periods of frequent outdoor activities, and prevention and management should be strengthened through active promotion.
Keywords: Lyme disease, Tick-borne diseases, Zoonotic diseases, Erythema migrans
Key messages
① What is known previously?
Lyme disease is a tick-borne zoonosis caused by Borrelia burgdorferi. It is an infectious disease that occurs when the pathogen spreads during the blood-sucking process of an infected tick.
② What new information is presented?
As the number of tick carriers increases due to climate change, the number of patients with Lyme disease and the areas where it occurs are expected to further expand. Although regional differences depending on climate (temperature, humidity, and rainfall) and environmental factors are observed, tick-borne Borrelia burgdorferi have already become indigenous.
③ What are implications?
Lyme disease is an infectious illness with a low fatality rate; however, if it does not receive appropriate treatment in the early stages, it can become a chronic disease. During the season of frequent outdoor activities, it is important to reduce exposure to ticks to avoid bites, and prevention and management must be strengthened through active promotion.
Introduction
Lyme disease is a tick-borne zoonotic illness in which tick larvae infected with bacteria of the genus Borrelia (Borrelia burgdorferi, Borrelia afzelii, and Borrelia garinii) enter the body when ticks penetrate human skin as they feed on blood to develop into nymphs the following summer [1].
In the United States, Lyme disease is the most common tick-borne illness, with an overall annual incidence of >30,000 individuals. Cases of Lyme disease have also been reported annually in the United Kingdom, Spain, Australia, Canada, Russia, China, and Japan [2]. In the Republic of Korea (ROK), 233 cases of Lyme disease have been exported until 2023 since the Lyme disease surveillance was initiated in 2011, with the number of reported cases ranging 10–20 per year, peaking at 45 in 2023. Without proper treatment in the early stages, Lyme disease can become chronic, resulting in neurological symptoms, encephalitis, and paralysis in 15% of untreated patients, cardiovascular symptoms in 8%, and chronic infections, such as monoarthritis and acrodermatitis chronica atrophicans, in approximately 60% of untreated patients, weeks or years after infection [3].
The global incidence of tick-borne diseases has been increasing, likely due to the expanding tick population caused by global warming [4]. With the detection of the causative agent of Lyme disease in ROK, Ixodes persulcatus, Ixodes nipponensis, and Ixodes granulatus [5], the number of cases is projected to increase. After isolating the pathogen from ticks in the early 1990s, the Korea Disease Control and Prevention Agency designated Lyme disease as a statutory notifiable disease in 2010 to monitor outbreaks and characterize its main attributes. In ROK, Lyme disease mainly occurs from May to November, and the number of domestic cases has at least tripled compared to the imported cases over the past 3–4 years. In this report, we provide fundamental data of Lyme disease for the prevention and control by analyzing epidemiological survey data reported in the past 5 years, 2019–2023.
Methods
In this investigation, we analyzed data from 116 cases of Lyme disease (29 confirmed and 87 suspected) reported to the Integrated Disease & Health Management System and reflected in the statistics for the past 5 years (January 1, 2019–December 31, 2023) through frequency analysis according to year, month, and region based on the report date. Cases of Lyme disease were classified as confirmed or suspected according to the 2023 Statutory Infectious Disease Diagnosis and Reporting Criteria [6]. Epidemiological survey data for these cases were comparatively analyzed according to epidemiological (such as time and risk factors of the exposure) and clinical (such as symptoms, underlying diseases, and medical treatment modalities) characteristics, which were divided into Korean domestic infection, imported, and unknown according to the origin of infection. The criteria used to distinguish domestic and international cases were epidemiological associations within 1 month before the manifestation of the first symptom, considering the incubation period of Lyme disease (3–30 days). Cases in which loss of contact and communication issues made it difficult to determine the origin of infection solely based on epidemiological findings were categorized as unknown.
Results
1. Reported Cases of Lyme Disease
A total of 116 cases of Lyme disease (84 domestically infected, 29 overseas-acquired, and three unknown) were reported between January 1, 2019 and December 31, 2023; the yearly distribution of these cases were as follows: 2019, n=23; 2020, n=18; 2021, n=8; 2022, n=22; and 2023, n=45. A distinct increase in the number of cases occurred in 2023 following the novel coronavirus disease (COVID-19) pandemic. In 2023, the number of imported cases remained <10, while the number of domestic cases increased to 36 (Figure 1A). Meanwhile, Lyme disease cases occurred between April and November, with the highest number of domestic cases (n=19 [16.4%]) reported in November (Figure 1B).
Figure 1. Lyme disease reporting status (2019–2023).
(A) By year. (B) By month.
2. Epidemiological Characteristics
Regarding the general characteristics of Lyme disease, there was no significant differences in terms of sex, with 56 males (48.3%) and 60 females (51.7%). The mean (±standard deviation [SD]) age was 44.0±17.7 years, with 39 (33.6%) cases ≥60 years of age; the majority of domestic cases were individuals ≥60 years of age (44.0%) while imported cases were mainly those 20–49 years of age (55.2%). Regarding occupation, 31 (26.7%) were householder/unemployed, of whom the most domestic cases were agricultural workers (25.0%), while most imported cases were 12 (41.4%) were householder/unemployed. A total of 116 patients were classified based on epidemiological characteristics, with 29 confirmed (25.0%) and 87 suspected (75.0%) cases, of whom 84.5% (n=98) were Koreans. According to season, 42 (36.2%) cases occurred in summer and autumn. The most domestic infections occurred in autumn (n=36 [42.9%]), while most foreign-borne infections occurred in summer (n=16 [55.2%]).
Regarding the history of outdoor activities, 54 (64.3%) of 84 domestically infected individuals were engaged in outdoor activities, including simple outdoor activity and farm/field work of 22 (40.7%) (Table 1).
Table 1. Characteristics of Lyme disease in Korea, 2019–2023.
| Categories | Total (n=116) | Domestic (n=84) | Imported (n=29) | Uncertainly (n=3) |
|---|---|---|---|---|
| Gender | ||||
| Male | 56 (48.3) | 42 (50.0) | 13 (44.8) | 1 (33.3) |
| Female | 60 (51.7) | 42 (50.0) | 16 (55.2) | 2 (66.7) |
| Age (yr)a) | (44.0±17.7) | (53.7±21.1) | (36.2±21.1) | (44.3±21.4) |
| ≤20 | 7 (6.0) | 5 (6.0) | 2 (6.9) | - |
| 20–39 | 14 (12.1) | 6 (7.1) | 8 (27.6) | - |
| 30–49 | 21 (18.1) | 12 (14.3) | 8 (27.6) | 1 (33.3) |
| 40–49 | 14 (12.1) | 10 (11.9) | 3 (10.3) | 1 (33.3) |
| 50–59 | 21 (18.1) | 14 (16.7) | 6 (20.7) | 1 (33.3) |
| ≥60 | 39 (33.6) | 37 (44.0) | 2 (6.9) | - |
| Occupation | ||||
| Agricultural worker | 21 (18.1) | 21 (25.0) | - | - |
| Office/specialized worker | 28 (24.1) | 17 (20.2) | 10 (34.5) | 1 (33.3) |
| Construction worker | 18 (15.5) | 13 (15.5) | 5 (17.2) | - |
| Householder/unemployed | 31 (26.7) | 19 (22.6) | 12 (41.4) | - |
| Other | 26 (22.4) | 14 (16.7) | 10 (34.5) | 2 (66.7) |
| Case classification | ||||
| Confirmed cases | 29 (25.0) | 21 (25.0) | 8 (27.6) | - |
| Probably | 87 (75.0) | 63 (75.0) | 21 (72.4) | 3 (100.0) |
| Nationalities | ||||
| Koreans | 98 (84.5) | 83 (98.8) | 14 (48.3) | 1 (33.3) |
| Foreigner | 18 (15.5) | 1 (1.2) | 15 (51.7) | 2 (66.7) |
| Season | ||||
| Spring (Mar–May) | 19 (16.4) | 16 (19.0) | 3 (10.3) | - |
| Summer (Jun–Aug) | 42 (36.2) | 25 (29.8) | 16 (55.2) | 1 (33.3) |
| Fall (Sep–Nov) | 42 (36.2) | 36 (42.9) | 6 (20.7) | - |
| Winter (Dec–Feb) | 13 (11.2) | 7 (8.3) | 4 (13.8) | 2 (66.7) |
| Outdoor activitiesb) | 57 (49.1) | 54 (64.3) | 3 (10.3) | - |
| Farm/field work | 23 (40.4) | 22 (40.7) | 1 (33.3) | - |
| Simple outdoor activityc) | 24 (42.1) | 22 (40.7) | 2 (66.7) | - |
| Others | 4 (7.0) | 4 (7.4) | - | - |
| Uncertainly | 6 (10.5) | 6 (11.1) | - | - |
| Staying or visiting abroad | 30 (25.9) | 1 (1.2) | 29 (100.0) | - |
Values are presented as number (%). a)Mean±standard deviation. b)57 out of 116 total patients were confirmed to have outdoor activities through epidemiological investigation (including duplicate responses). c)6 hiking, 6 visiting graves and weeding, 5 walking around the area, 2 camping, 1 each on a golf course, fishing, and early morning soccer, and 2 others.
3. Clinical Characteristics
Clinical symptoms included fever (n=65 [56.0%]), erythema migrans/rash (n=61 [52.6%]), chills (n=35 [30.2%]), headache (n=34 [29.3%]), myalgia (n=32 [27.6%]), fatigue (n=27 [23.3%]), and arthralgia (n=18 [15.5%]) among a total of 116 patients. Fever (n=56 [66.7%]) and erythema migrans/rash (n=15 [51.7%]) were the most common symptoms among domestic and imported cases of Lyme disease, respectively. Underlying medical conditions were found in 31 (26.7%) individuals, of which the most common was hypertension (n=17 [14.7%]) followed by diabetes (n=7 [6.0%]). In addition, the mean (±SD) number of days from the first symptom to reporting to a healthcare facility was 17.4±18.6 days, which was longer for imported cases (19.2±19.8 days) than for domestic cases (16.2±18.1 days). According to treatment type, 59 (52.2%) and 54 (47.8%) individuals were treated through outpatient care and hospitalization, respectively. The mean length of hospitalization was 10.1±10.6 days, in which imported cases (20.0±18.0 days) had longer hospital stays than domestic cases (9.8±9.8 days) (Table 2).
Table 2. Clinical features of Lyme disease in Korea, 2019–2023.
| Categories | Total (n=116) | Domestic (n=84) | Imported (n=29) | Uncertainly (n=3) |
|---|---|---|---|---|
| Clinical featuresa) | ||||
| Fever | 65 (56.0) | 56 (66.7) | 7 (24.1) | 2 (66.7) |
| Erythema migrans/rash | 61 (52.6) | 44 (52.4) | 15 (51.7) | 2 (66.7) |
| Chills | 35 (30.2) | 29 (34.5) | 5 (17.2) | 1 (33.3) |
| Headache | 34 (29.3) | 27 (32.1) | 7 (24.1) | - |
| Myalgia | 32 (27.6) | 23 (27.4) | 9 (31.0) | - |
| Fatigue | 27 (23.3) | 19 (22.6) | 8 (27.6) | - |
| Arthralgia | 18 (15.5) | 10 (11.9) | 7 (24.1) | 1 (33.3) |
| Arthritis | 12 (10.3) | 6 (7.1) | 5 (17.2) | 1 (33.3) |
| Cardiovasxular symtom | 5 (4.3) | 4 (4.8) | 1 (3.4) | - |
| Neurology symptom | 6 (5.2) | 5 (6.0) | 1 (3.4) | - |
| 2nd Erythema migran | 3 (2.6) | 3 (3.6) | - | - |
| Lymphatic hypertrophy | 3 (2.6) | 2 (2.4) | 1 (3.4) | - |
| From symptom onset to reporting (day)c) | 17.4±18.6 | 16.2±18.1 | 19.2±19.8 | 23.5±4.8 |
| Underlying diseasesa) | 31 (26.7) | 29 (34.5) | 2 (6.9) | - |
| Hypertension | 17 (14.7) | 16 (19.0) | 1 (3.4) | - |
| Diabetes | 7 (6.0) | 7 (8.3) | - | - |
| Cerebrovascular diseases | 2 (1.7) | 2 (2.4) | - | - |
| Heart disease | 3 (2.6) | 3 (3.6) | - | - |
| Blood disease | 2 (1.7) | 2 (2.4) | - | - |
| Immunodeficiency disease | 3 (2.6) | 2 (2.4) | 1 (3.4) | - |
| Liver disease | 2 (1.7) | 2 (2.4) | - | - |
| Cancer | 2 (1.7) | 2 (2.4) | - | - |
| Others | 9 (7.8) | 9 (10.7) | - | - |
| Administrationb) | 113 (97.4) | 83 (98.8) | 27 (93.1) | 3 (100.0) |
| Ambulatory care | 59 (52.2) | 35 (42.2) | 22 (81.5) | 2 (66.7) |
| Hospitalization | 54 (47.8) | 48 (57.8) | 5 (18.5) | 1 (33.3) |
| Hospitalization period (day)c) | 10.1±10.6 | 9.8±9.8 | 20.0±18.0 | 3.0±0.0 |
Values are presented as number (%). a)Clinical features and Underlying disease can be duplicated. b)35 patients with confiemed hospitalization and discharge records as a result of epidemiological investigation. c)Mean±standard deviation.
4. Domestic Cases of Lyme Disease according to Year and City/Province
In ROK, 84 cases of Lyme disease were reported between 2019 and 2023. By province, Chungcheongnam-do had the highest number of cases (n=19 [22.6%]), followed by Gyeonggi-do (n=16 [19.0%]), Seoul (n=12 [14.3%]), and Incheon (n=10 [11.9%]) (Figure 2F). The number of cases decreased to six in 2021 and then increased to 16 in 2022, and 36 in 2023 (Figure 2A–E) by year.
Figure 2. Regional distribution of estimated areas of 84 cases Lyme disease in domestic by 2019–2023.
(A) 2019 (n=12). (B) 2020 (n=14). (C) 2021 (n=6). (D) 2022 (n=16). (E) 2023 (n=36). (F) 2019–2023 (n=84).
5. Countries of Origin for Foreign-borne Cases
From 2019 to 2023, there were 29 imported cases of Lyme disease. According to year, the number of cases increased from 2021, with the highest in 2023 (n=9 [31.0%]). The highest number of cases were from the United States (n=9 [31.0%]) and Germany (n=3 [10.3%]), while other countries in Europe, Asia, and elsewhere also contributed (Table 3).
Table 3. Estimated countries of Lyme disease, 2019–2023.
| Year | Case (n=29)a) | Country |
|---|---|---|
| 2019 | 9 (31.0) | USA (5), Sweden (1), Thailand (1), France (1), Hong Kong (1) |
| 2020 | 3 (10.3) | Germany (1), Eeast Europe (1), Austria (1) |
| 2021 | 2 (6.9) | USA (1), Russia (1) |
| 2022 | 6 (20.7) | USA (2), Germany (1), Mongolia (1), Vietmam (1), Togo (1) |
| 2023 | 9 (31.0) | USA (1), Germany (1), Russia (1), Romania (1), Belgium (1), India (1), Croatia (1), Thailand (1), Poland (1) |
Values are presented as number (%). a)Patients with Lyme disease who, as a result of epidemiological investigation, have not been exposed to domestic risks within the incubation period (3–30 days) and have been confirmed to have stayed or visited overseas.
Discussion
Over the past 5 years (2019–2023), the number of cases of Lyme disease declined during the COVID-19 pandemic in 2021 (n=8), and 2022 (n=22) and then increased in 2023 (n=45), likely due to a return to normal life and increased outdoor activity. The pattern of Lyme disease cases in the past 5 years was somewhat different from that in the previous 8 years of reported cases, from 2011 to 2018 [7]. In the past 4 years, domestic infections accounted for 72.4%, compared with 56.4% from 2011 to 2018. From 2011 to 2018, most domestic cases occurred in Chungcheongnam-do, Gyeonggi-do, Gangwon-do, and Gyeongsangnam-do, while in the past 5 years, additional cases were reported in Jeollanam-do, indicating that the pattern of Lyme disease has changed along with the increase in the number of cases.
The majority of Lyme disease cases occurred between June and November (72.4%), with the highest proportion occurring in November (16.4%). The density of hard ticks in ROK is reported to be high in May and June, when the number of nymphs is high, and in August and September, when the number of larvae is high, with a sharp decline in October [8]. Despite the sharp decline in the hard tick population in October, the number of cases increased in November. Considering that the incubation period of Lyme disease (3–30 days) is longer than that of other vector-borne diseases and that the initial symptoms are mild and early differential diagnosis of individuals with various febrile diseases is difficult [9], it is estimated that the period from exposure to ticks to the onset of symptoms and the period from symptom onset to diagnosis may have affected the increase. However, an additional follow-up studies should be conducted to clarify the exact causes.
In ROK, Lyme disease caused by domestic infection was reported in nine of 17 cities and provinces except Daegu, Ulsan, Sejong, and Jeju. I. nipponensis and Haemaphysalis japonica, the vectors of Lyme disease, have been collected in all regions of the country except Gangwon-do (Inje), Gyeonggi-do (Gwangju), Jeollanam-do (Boseong), and Jeju-do [8]. Despite regional differences from climatic (such as temperature, humidity, and precipitation) and environmental factors, Lyme disease-carrying ticks appear to have already become indigenized in the country. Therefore, to reduce tick exposure and prevent tick bites during seasons of frequent outdoor activities, it is critical to strengthen the prevention and management strategies through rigorous active campaigns. Moreover, further researches are needed to investigate the relationship between the distribution of Lyme disease-carrying ticks and occurrence of Lyme disease in the country through the collection of ticks in presumed areas with high infection rates.
The number of imported cases of Lyme disease has increased since 2021, with the highest number in 2023 (n=9 [31.0%]). The United States accounted for the largest proportion of imported cases (31.0%), followed by Germany (10.3%), Thailand (6.9%), and other countries. Lyme disease is a tick-borne illness that occurs primarily in North America, Europe, and Asia, with 173,773 cases of Lyme disease in the United States during 2018–2022, representing a 15.4% increase in 2022 compared with that in 2021 [10]. This increase could be attributed to the increased chances for exposure to the tick vector, resulting from increased international travel and stays after COVID-1 pandemic, and it is believed that the cases were introduced into the country during the incubation period after exposure to ticks during international travel and stays. Therefore, it is necessary to provide advice and guidance on Lyme disease to travelers visiting areas where Lyme disease is likely to occur, as well as to monitor for imported cases.
Lyme disease can usually be completely cured if the infected individuals are treated with antibiotics at an early stage. However, if diagnosis is delayed or antibiotic treatment is inappropriate, Lyme disease can invade and negatively affect the organ systems including the nervous system (meningitis and encephalitis), heart (arrhythmia), and musculoskeletal system (arthritis). Especially among immunocompromised patients, Lyme disease can cause death in rare cases [11]. Patients with suspected symptoms of Lyme disease should be examined in healthcare facilities for history of outdoor activities or international travel for early diagnosis and appropriate treatment, for which further researches are needed to improve control measures.
In ROK, the most common origin of Lyme disease was domestic infection (72.4%), which was not predominantly associated with a specific occupation or age group but mainly related to various outdoor activities. The numbers of domestic cases and outbreak areas are expected to expand with an increase in vector populations due to climate change. Therefore, it is important to promote the prevention strategies and education to the public as well as overseas travelers to visit a medical institution immediately if they have symptoms, such as erythema migrans, after outdoor activities such as hiking in the mountains and/or activities in parks and fields.
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: KDH. Data curation: KDH, LSK. Formal analysis: KDH. Investigation: KDH. Methodology: KDH, HJH, KJH. Project administration: KJH. Supervision: KJH, KJH. Validation: KJH. Visualization: KDH. Writing – original draft: KDH. Writing – review & editing: KJH.
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