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Distribution Survey of Babesia and Assessment of Tick-borne Diseases in Jeju, Republic of Korea
Korean J Clin Lab Sci 2024;56:189-197  
Published on September 30, 2024
Copyright © 2024 Korean Society for Clinical Laboratory Science.

Jiro KIM1,2 and YoungMin YUN2

1Department of Clinical Laboratory Science, Cheju Halla University, Jeju, Korea
2College of Veterinary Medicine and Veterinary Medical Research Institute, Jeju National University, Jeju, Korea
Correspondence to: YoungMin YUN
College of Veterinary Medicine and Veterinary Medical Research Institute, Jeju National University, 102 Jejudaehak-ro, Jeju 63243, Korea
E-mail: dvmyun@jejunu.ac.kr
ORCID: https://orcid.org/0000-0003-0695-0843
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
From March to November 2021, a study conducted in Jeju used the dry ice trap method to collect 17,855 ticks across six regions, examining their distribution and potential as disease vectors. The ticks were identified and categorized by species and growth stage. In addition, the study focused on Babesia, a disease transmitted by hard ticks. Of 17,641 ticks from which DNA had been extracted, 581 pools underwent polymerase chain reaction testing. Of these, 43 pools tested positive for Babesia, with the highest positivity found in Western Seogwipo (23 pools, 53.5%), followed by eastern Seogwipo and central Jeju. The peak times for positive results were April and July. This study highlights an increased risk of tick bites linked to the rising number of abandoned pets in Jeju, necessitating ongoing environmental management and monitoring. These findings provide fundamental data for formulating strategies to prevent and manage tick-borne diseases in Jeju. This involves reducing the disease incidence through targeted preventive measures and detailed epidemiological research. These results underscore the necessity for continued vigilance and proactive intervention to address the health challenges ticks pose in the region.
Keywords : Babesia, Disease vectors, Polymerase chain reaction, Public health, Tick-borne diseases
INTRODUCTION

The introduction of new infectious diseases into Korea is being accelerated by increased overseas travel and international exchanges. The World Health Organization has highlighted that global warming is causing significant changes in the distribution and habitats of disease vectors such as mites and mosquitoes, altering their species composition and population dynamics [1]. As a consequence of climate change, vectors traditionally confined to tropical regions are now able to survive in Korea, elevating the risk of tick and mosquito-borne diseases becoming more widespread. This poses a particular threat to Jeju Island, at Korea’s southern extremity, where the introduction of novel vectors could potentially lead to a higher incidence of new infectious diseases compared to other areas [2].

Ticks, which are classified into hard ticks and mites, play a crucial role as carriers of various diseases. Hard ticks, measuring about 1 to 3 mm, are known vectors for Lyme disease, severe fever with thrombocytopenia syndrome (SFTS), anaplasmosis, ehrlichiosis, Q fever, and babesiosis. Mites, smaller in size (0.1∼0.3 mm) and primarily parasitizing wild mice, are recognized for transmitting scrub typhus [3]. The hard tick, operating as a three-host tick, undergoes four life stages: egg, larva, nymph, and adult. In Korea, notable species include Haemaphysalis longicornis, Haemaphysalis flava, Ixodes persulcatus, and Ixodes nipponensis, with H. longicornis comprising 92% to 96% of the tick population. These species predominantly parasitize wild animals, rodents, and birds, posing a significant risk of disease transmission to humans. Reported diseases in Korea encompass erlichiosis, anaplasmosis, Q fever, tsutsugamushi disease, and SFTS [4-7].

The ongoing rise in global temperatures fosters a more conducive environment for ticks, leading to heightened tick activity and an increase in tick-borne diseases. Concurrently, the surge in pet ownership is contributing to a rise in pets infected with these diseases [8]. Among tick-borne diseases, babesiosis is particularly noteworthy. This disease, observed in rodents, humans, dogs, cats, horses, and cattle, is characterized by the presence of protozoans in red blood cells, most commonly detected in dogs [9]. This study aims to explore the distribution of ticks across Jeju Island and assess the infection rate of Babesia, illustrating the broader implications of tick-borne diseases in the region.

MATERIALS AND METHODS

1. Tick Collection

Jeju Island is divided into six administrative districts. For this study, we selected representative areas within these districts, with a focus on regions where livestock grazing occurs. This selection aimed to represent the diverse ecosystems of Jeju Island and reflect the characteristics of each administrative district. By doing so, we intended to accurately analyze the distribution and characteristics of ticks across various environments. Pyeongdae-ri, Gujwa-eup (33°26′41.6″N 126° 45′19.6″E) represented the eastern part of Jeju, and Yonggang-dong (33°28′02.7″N 126°35′47.4″E) the central part. Geumak-ri, Hallim-eup (33°21′17.9″N 126°19′48.8″E) was chosen for the western part of Jeju. For Seogwipo, Gashi-ri, Pyoseon-myeon (33°25′50.4″N 126°43′28.1″E) was selected for the eastern part, Donghong-dong (33°17′20.7″N 126°33′27.3″E) for the central part, and Gueok-ri, Daejeong-eup (33°16′44.4″N 126°15′51.9″E) for the western part, all in 2021. The collection was conducted from March to November (Figure 1). As for the method of collection, the dry-ice bait trap method was employed, setting up two traps at 50 m intervals in each area between 15:00 and 17:00 the day before collection, and collecting them between 9:00 and 11:00 the next day [2].

Fig. 1. Collecting site of hard tick in Jeju.

2. Tick Identification

Upon documenting the characteristics of the collection site, species identification was conducted through classification, including collection date and location. This identification process utilized a dissecting microscope (Olympus), adhering to the guidelines provided by Yamaguti et al [10]. The specimens—larvae, nymphs, adult males, and adult females were categorized based on species identification and their developmental stage. Subsequently, half of the specimens were preserved in 100% alcohol, while the other half were allocated for disease identification (Figure 2).

Fig. 2. Identification of tick species in Jeju.

3. DNA Extraction and Polymerase Chain Reaction

For DNA extraction and polymerase chain reaction (PCR) analysis, the 8,419 ticks collected were grouped into pools of 5 adults, 30 nymphs, and 50 larvae each. Each pool was then treated with 350 μL of lysis buffer and homogenized using the BEAD RUPTOR ELITE (PerkinElmer) for 30 seconds across 2 cycles. DNA extraction was conducted using the Patho Gene-spin DNA/RNA Extraction Kit (iNtRON Biotechnology), following the provided instructions. To detect Babesia, a PCR assay was performed using the BIO-RAD T100 Thermal Cycler (Bio-Rad Laboratories). For the amplification of Babesia spp. 18s rRNA, the PCR reaction mixture was prepared with 1 μL of forward primer (10 pmol/μL), 1 μL of reverse primer (10 pmol/μL), 10 μL of 2X PCR Pre-Mix, 5 μL of template DNA, and 3 μL of distilled water, for a total volume of 20 μL. The forward primer sequence used was 5′-GACACAGGGAGGTAGTGACAAG-3′ and the reverse primer sequence used was 5′-CTAAGCATTTCACCTCTGACAGT-3′. The PCR conditions included an initial denaturation at 95℃ for 3 minutes, followed by 34 cycles of denaturation at 95℃ for 30 seconds, annealing at 55℃ for 30 seconds, and extension at 72℃ for 30 seconds, with a final extension at 72℃ for 2 minutes. The expected size of the PCR product was approximately 403 bp. To verify the presence of amplified Babesia DNA, agarose gel electrophoresis was conducted using a gel composed of 0.6 g agarose, 40 mL TBE buffer, and 2 μL red safe, running at 100 V for 20 minutes (Figure 3).

Fig. 3. Result of Babesia polymerase chain reaction.
Abbreviations: M, marker; P, positive control; 1∼4, samples; N, negative control.
RESULTS

1. Distribution of Ticks in Jeju

Excluding the 8,041 (45.0%) larvae that were difficult to identify, a total of 9,751 (54.6%) H. longicornis and 63 (0.4%) H. flava ticks were collected. In the classification by growth stage of H. longicornis, 770 (4.3%) were adult males, 1,267 (7.1%) were adult females, and 7,714 (43.2%) were nymphs. For H. flava, 13 adult males (0.1%), 3 adult females (less than 0.1%), and 47 nymphs (0.3%) were collected. Additionally, 8,041 (45.0%) larvae were gathered (Table 1). The monthly distribution showed 277 ticks in March, 1,078 in April, 1,877 in May, 2,694 in June, 2,493 in July, 2,331 in August, 5,487 in September, 1,468 in October, and 150 in November (Figure 4). By region, the collection included 8,774 (49.1%) from western Seogwipo, 3,532 (19.8%) from eastern Seogwipo, 3,708 (20.8%) from central Seogwipo, 187 (1.0%) from western Jeju, 887 (5.0%) from eastern Jeju, and 767 (4.3%) from central Jeju (Table 2).

Fig. 4. Monthly distribution of hard tick in Jeju.
Abbreviations: H. longicornis, Haemaphysalis longicornis; H. flava, Haemaphysalis flava; M, male; F, female.

Distribution of hard tick by month in JeJu

Haemaphysalis longicornis Haemaphysalis flava Larva Total


Adult (M) Adult (F) Nymph Adult (M) Adult (F) Nymph
March 9 2 261 - 2 2 1 277
April 28 31 1,006 2 - 10 1 1,078
May 123 112 1,614 1 1 26 - 1,877
June 198 406 2,089 - - 1 - 2,694
July 284 467 992 - - - 750 2,493
August 116 209 701 3 - - 1,302 2,331
September 5 35 956 2 - - 4,489 5,487
October 4 - 87 2 - 4 1,371 1,468
December 3 5 8 3 - 4 127 150
Total 770 1,267 7,714 13 13 3 47 8,041 17,855

Abbreviations: M, male; F, female; -, not applicable.



Distribution of hard tick by region in Jeju

Haemaphysalis longicornis Haemaphysalis flava Larva Total
Eastern Seogwipo 2,268 7 1,257 3,532
Western Seogwipo 5,066 21 3,687 8,774
Central Seogwipo 1,525 34 2,149 3,708
Eastern Jeju 337 1 549 887
Western Jeju 147 0 40 187
Central Jeju 408 0 359 767


2. Polymerase Chain Reaction Result of Babesia

From March to October 2021, DNA was extracted from 8,922 of the 17,641 ticks, forming 581 pools, and PCR tests for Babesia were conducted. Babesia was detected in a total of 43 pools, yielding a minimum infection rate of 0.48%. By species and growth stage, Babesia was found in 9 out of 111 pools of H. longicornis adult males and in 9 out of 153 pools of adult females, as well as in 16 out of 191 pools of nymphs, making a total of 34 positive pools out of 455 tested pools. Babesia was detected in 4,952 specimens, including 393 adult males, 651 adult females, and 3,908 nymphs, with a minimum infection rate of 0.69%. For H. flava, Babesia was detected in only 1 pool of adult males out of 21 pools, totaling 34 ticks, and the minimum infection rate was 2.94%. Among larvae, totaling 3,936 ticks, Babesia was detected in 8 out of 105 pools, with a minimum infection rate of 0.2% (Table 3). Regionally, Babesia positive results were found in 23 pools (53.5%) in western Seogwipo, 7 pools (16.3%) in eastern Seogwipo, 4 pools (9.3%) in central Seogwipo, 0 pools (0.0%) in western Jeju, 4 pools (9.3%) in eastern Jeju, and 5 pools (11.6%) in central Jeju (Figure 5). Monthly, the highest positivity rates were observed in April with 16 pools (37.2%), followed by July with 14 pools (32.6%), September with 8 pools (18.6%), and June with 5 pools (11.6%) (Table 4).

Fig. 5. Detection rate of Babesia by region in Jeju.

Detection rate of Babesia in hard ticks from Jeju

Tick species Stage No. of ticks No. of pools No. of infected Babesia MIR
Haemaphysalis longicornis Adult (M) 393 111 9 2.29
Adult (F) 651 153 9 1.38
Nymph 3,908 191 16 0.41
Subtotal 4,952 455 34 0.69
Haemaphysalis flava Adult (M) 9 7 1 11.11
Adult (F) 4 4 - 0.00
Nymph 21 10 - 0.00
Subtotal 34 21 1 2.94
Haemaphysalis spp. Larva 3,936 105 8 0.20
Total 8,922 581 43 0.48

Abbreviations: MIR, minimum infection rate per 100 ticks; M, male; F, female; -, not detected.



Number of detections of Babesia in hard tick by month and region in Jeju

Number of positive pools

March April May June July August September October
Eastern Seogwipo 0 5 0 2 0 0 0 0
Western Seogwipo 0 9 0 1 8 0 5 0
Central Seogwipo 0 1 0 2 0 0 1 0
Eastern Jeju 0 1 0 0 2 0 1 0
Western Jeju 0 0 0 0 0 0 0 0
Central Jeju 0 0 0 0 4 0 1 0
Total 0 16 0 5 14 0 8 0

DISCUSSION

Ticks are found worldwide, including in regions such as Asia, Europe, America, Africa, and Korea. The prevalence of tick-borne diseases is escalating, largely due to the effects of global warming. In Korea, there’s a noticeable pattern in tick density according to their growth stages: nymphs are predominantly collected in the spring months of April to May, adults from late spring through to summer (May to July), and larvae are usually gathered in the early autumn, particularly in September [11].

According to the report from the Division of Vector Analysis, Bureau of Infectious Disease Diagnosis and Analysis, Korea Disease Control and Prevention Agency [12], the Babesia species that can infect humans traditionally include Babesia microti, Babesia divergens, Babesia venatorum, and Babesia duncani, with B. microti accounting for the majority of infections. Additionally, the primary vectors transmitting Babesia to humans are ticks of the Ixodidae family, particularly those of the genus Ixodes. However, human cases of Babesia infection in Korea are extremely rare, with no reported cases from Jeju specifically. This indicates that the presence of Babesia-positive ticks found in this study does not necessarily imply a significant risk of human infection. Nevertheless, these findings provide essential baseline data for local surveillance and prevention strategies [12].

Upon examining 17,855 ticks by species and growth stage, and excluding 8,041 larvae (45.0%) that were difficult to identify, it was found that H. longicornis, making up 54.6% of the collection, is the dominant tick species in Korea. A smaller percentage, 0.4%, was identified as H. flava, which aligns with findings from other studies. It is generally observed that tick populations increase during the autumn months, from September to November [13].

Larvae collection commenced in July, the peak of the summer season, revealing that tick distribution varies with the seasons, depending on the growth stage [2]. A focused study on Babesia, a disease caused by tick-borne pathogens, involved extracting DNA from 581 pools (comprising 8,922 ticks) and performing PCR tests for babesia detection. The results showed that babesia was present in 43 pools. Notably, western Seogwipo exhibited a high infection rate, with 8,634 (50.7%) ticks collected from this region alone, indicating a significantly high rate of infection. This suggests that Babesia infects ticks across the entirety of Jeju. While Babesia predominantly affects dogs, it is recognized as a zoonotic pathogen that can also infect humans. Tick-borne diseases that can be transmitted include Ehrlichiosis, scrub typhus (Orientia tsutsugamushi), Lyme disease (Borrelia), and SFTS. The causative agents of these diseases include Borrelia spp., Bartonella spp., parasitic Rickettsia (Rickettsia spp.), Ehrlichia spp., Anaplasma spp., tick-borne encephalitis virus, severe fever with thrombocytopenia syndrome virus, and the protozoan Babesia spp. [14].

Recent years have seen an increase in abandoned and feral dogs in Jeju, raising concerns over tick bites during outdoor activities and the subsequent risk of transmission to humans from pets. This situation underscores the need for continuous monitoring and effective environmental management strategies [15]. The peak infection rates observed in April correspond with the periods of increased tick activity, typically from April to May and September to October, emphasizing the importance of preventive measures against tick bites during spring and autumn [9]. The rising global temperatures and increased international travel necessitate vigilant monitoring and proactive preventive measures to curb the spread of tick-borne diseases [16].

The 18s rRNA gene was targeted for the amplification of Babesia spp. instead of the 16s rRNA gene for several reasons. The 16s rRNA gene is commonly used for the identification and phylogenetic studies of bacteria and archaea due to its conserved and variable regions that allow for the differentiation of diverse bacterial species. However, Babesia spp. are protozoa, belonging to the eukaryotic domain, making the 18s rRNA gene a more appropriate target [14].

The 18s rRNA gene is a well-conserved genetic marker within eukaryotes, including protozoa, and is extensively used for phylogenetic studies and species identification [15]. Its high conservation across eukaryotic organisms allows for the reliable detection and differentiation of various Babesia species. Additionally, the 18s rRNA gene provides a higher sensitivity and specificity in PCR assays, enabling the effective detection of low concentrations of Babesia DNA [9].

By targeting the 18s rRNA gene, this study ensures a more accurate identification of Babesia spp., contributing to the understanding of the phylogenetic relationships among different Babesia species and facilitating the discovery of new species. This choice of genetic marker enhances the diagnostic precision and supports the development of better surveillance and control strategies for Babesia infections.

Internationally, human cases of Babesia infection have been reported in various countries, showing that it is not a localized issue. In the United States, B. microti is the most commonly reported species causing human infection. European countries report infections primarily due to B. divergens and B. venatorum. These international cases highlight the zoonotic potential of Babesia species and the need for global awareness and control measures [17-19].

In this study, the highest infection rates in Jeju were observed in western Seogwipo, with peak infection periods in April and July. This coincides with increased outdoor activities during the summer months, suggesting a correlation between human exposure and tick activity. Therefore, public health strategies should emphasize the importance of tick bite prevention, particularly during these peak activity periods.

As engagement in outdoor activities such as hiking, walking, and camping rises, so too does the potential for tick encounters, highlighting the importance of adhering to preventive measures against tick bites. The most effective strategy to prevent tick bites is to avoid being bitten. Protective measures include wearing gloves, long socks, hats, long sleeves, long pants, hiking boots, using repellents, avoiding grassy areas, using an air gun to remove ticks from clothing or the body, showering, and washing outdoor clothes separately [20].

This study has provided a comprehensive analysis of tick distribution and the babesia infection rate in Jeju. It aims to serve as a foundation for future research into other tick-borne diseases such as SFTS, Ehrlichia, and Borrelia, potentially contributing to the prevention and management of tick-borne diseases in Jeju. Furthermore, it is hoped that these findings will assist in the epidemiological study of tick-borne diseases, aiding in their prevention and reducing the incidence of infectious diseases.

요 약

본 연구에서는 2021년 3월부터 11월까지 제주를 6개 지역으로 나누어 드라이아이스 유인트랩 방법을 이용하여 총 17,855마리의 참진드기를 채집하여 분포와 매개질병 잠재력을 조사하였다. 채집된 참진드기는 종과 성장단계별로 동정 및 분류되었으며, 참진드기가 매개하는 대표적인 질병인 Babesia에 대해 분석하였다. 채집된 참진드기 중 DNA가 추출된 17,641마리에서 581 pools에 대한 PCR 검사를 진행하여, 이 중 43 pools에서 Babesia 양성 반응을 보였다. 양성 반응은 지역별로 서귀포시 서부에서 가장 높게 나타났으며(23 pools, 53.5%), 이어서 서귀포시 동부와 제주시 중부에서도 확인되었다. 월별 양성률은 4월과 7월에 가장 높았다. 최근 제주에서 유기견과 반려견의 증가로 인해 야외활동 중 진드기에 물릴 위험이 증가하고 있으며, 이로 인한 감염이 사람에게 전파될 가능성이 있어 지속적인 모니터링과 환경 관리의 필요성이 강조된다. 이 연구 결과는 제주 지역에서 진드기 매개 질병의 예방 및 관리 전략 수립에 있어 기초 데이터로 활용될 것이며, 감염병 예방과 역학 조사에 기여할 것으로 기대된다.

Acknowledgements

We express our gratitude to the Didimdol Scholarship Foundation of Seogwipo JungAng Church for their generous support. Deep gratitude is extended to Professor YoungMin Yun’s laboratory team, including Bum-Seok Kim and Jeong-Min Seo, from the College of Veterinary Medicine, Jeju National University, for their invaluable assistance in data collection and analysis. Special thanks are also due to Professor Yun, the corresponding author and advisor, for his continuous support and guidance throughout this study.

Funding

This research was supported by the Korea Disease Control and Prevention Agency (Fund Management Number: 6332-305-210) for the project titled “Climate Change Vector Surveillance Center (JeJu)”. Additionally, this work was funded by the Animal and Plant Quarantine Agency (Project Number: Z-1543081-2019-21-01) for the project titled “Establishment of the Monitoring System of Ticks and Tick-borne Livestock Diseases in Korea”.

Conflict of interest

None

Author’s information (Position)

Kim J1,2, Professor; Yun YM2, Professor.

Author Contributions

-Conceptualization: Yun YM.

-Data curation: Kim J.

-Formal analysis: Kim J.

-Methodology: Kim J, Yun YM.

-Software: Kim J.

-Validation: Kim J, Yun YM.

-Investigation: Kim J, Yun YM.

-Writing - original draft: Kim J, Yun YM.

-Writing - review & editing: Kim J, Yun YM.

Ethics approval

This article does not require IRB/IACUC approval because there are no human and animal participants.

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