Molecular detection of Anaplasma phagocytophilum in field-collected Haemaphysalis larvae in the Republic of Korea

Abstract Background Anaplasma spp., zoonotic tick-borne pathogens affecting livestock, companion animals, and humans, exhibits 15–18% seropositivity among hunting dogs in the Republic of Korea (South Korea). The dominant tick species in South Korea, Haemaphysalis longicornis, can transmit these path...

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Main Authors: KyuSung Ahn, Badriah Alkathiri, Seung-Hun Lee, Haeseung Lee, Dongmi Kwak, Yun Sang Cho, Hyang-Sim Lee, SoYoun Youn, Mi-Sun Yoo, Jaemyung Kim, SungShik Shin
Format: Article
Language:English
Published: BMC 2025-02-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-024-06649-z
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author KyuSung Ahn
Badriah Alkathiri
Seung-Hun Lee
Haeseung Lee
Dongmi Kwak
Yun Sang Cho
Hyang-Sim Lee
SoYoun Youn
Mi-Sun Yoo
Jaemyung Kim
SungShik Shin
author_facet KyuSung Ahn
Badriah Alkathiri
Seung-Hun Lee
Haeseung Lee
Dongmi Kwak
Yun Sang Cho
Hyang-Sim Lee
SoYoun Youn
Mi-Sun Yoo
Jaemyung Kim
SungShik Shin
author_sort KyuSung Ahn
collection DOAJ
description Abstract Background Anaplasma spp., zoonotic tick-borne pathogens affecting livestock, companion animals, and humans, exhibits 15–18% seropositivity among hunting dogs in the Republic of Korea (South Korea). The dominant tick species in South Korea, Haemaphysalis longicornis, can transmit these pathogens to both humans and animals. Given the limited understanding of transovarial transmission of Anaplasma spp., our study aimed to assess the prevalence of questing larval ticks containing Anaplasma DNA. Additionally, we aimed to gather data for establishing a nationwide forecasting and alert system on seasonal variation of tick developmental stages and tick-borne zoonotic pathogens. Methods From March to October 2021 and again from March to October 2022, we collected a total of 36,912 unfed, questing ticks of Haemaphysalis spp. from 149 sites in South Korea. Ticks were collected from herbaceous vegetation using the flagging method using a white flannel cloth. After species identification, one-third of collected ticks underwent analysis for Anaplasma DNA. Nymph ticks were pooled in groups of 1–10 and larvae in groups of 1–50, while adults were examined individually. Nested polymerase chain reaction (PCR) was performed to detect the genus Anaplasma by amplifying the 16S rRNA gene, followed by sequencing for species identification and phylogenetic analysis. Results Of the 36,912 questing ticks collected, 13,082 (35.4%) were identified as nymphs and adults of H. longicornis and 3850 (10.4%) as those of Haemaphysalis flava. The morphologically indistinguishable larval stage of Haemaphysalis spp. predominated, with 19,980 (54.1%) collected primarily from July to October. From the 939 tick pools, 24 pools (2.6%) tested positive for Anaplasma, with the larval stage exhibiting the highest number of positive pools (16, 1.7%). Phylogenetic analysis revealed that 21 of the 24 Anaplasma-positive pools contained A. phagocytophilum-specific genes, with 1 identified as Anaplasma sp. and the remaining 2 as A. bovis. Conclusions Our study provides evidence of transovarial transmission of A. phagocytophilum in Haemaphysalis spp. larvae under field conditions, showing that the bacteria are transmitted from mother ticks to unengorged, questing larvae. Additionally, our findings contribute significant data for establishing a nationwide forecasting and alert system on seasonal variation of tick developmental stages and tick-borne zoonotic pathogens. Graphical Abstract
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spelling doaj-art-4c7744775bbd46aabeb6f16d5d8e22e32025-08-20T02:15:06ZengBMCParasites & Vectors1756-33052025-02-011811910.1186/s13071-024-06649-zMolecular detection of Anaplasma phagocytophilum in field-collected Haemaphysalis larvae in the Republic of KoreaKyuSung Ahn0Badriah Alkathiri1Seung-Hun Lee2Haeseung Lee3Dongmi Kwak4Yun Sang Cho5Hyang-Sim Lee6SoYoun Youn7Mi-Sun Yoo8Jaemyung Kim9SungShik Shin10BIOREEDS Research Institute, College of Veterinary Medicine, Chonnam National UniversityCollege of Veterinary Medicine, Chungbuk National UniversityCollege of Veterinary Medicine, Chungbuk National UniversityCollege of Veterinary Medicine, Kyungpook National UniversityCollege of Veterinary Medicine, Kyungpook National UniversityViral Disease Division, Department of Animal and Plant Health Research, Animal and Plant Quarantine AgencyParasitic and Honeybee Disease Laboratory, Bacterial Disease Division, Department of Animal and Plant Health Research, Animal and Plant Quarantine AgencyParasitic and Honeybee Disease Laboratory, Bacterial Disease Division, Department of Animal and Plant Health Research, Animal and Plant Quarantine AgencyParasitic and Honeybee Disease Laboratory, Bacterial Disease Division, Department of Animal and Plant Health Research, Animal and Plant Quarantine AgencyParasitic and Honeybee Disease Laboratory, Bacterial Disease Division, Department of Animal and Plant Health Research, Animal and Plant Quarantine AgencyBIOREEDS Research Institute, College of Veterinary Medicine, Chonnam National UniversityAbstract Background Anaplasma spp., zoonotic tick-borne pathogens affecting livestock, companion animals, and humans, exhibits 15–18% seropositivity among hunting dogs in the Republic of Korea (South Korea). The dominant tick species in South Korea, Haemaphysalis longicornis, can transmit these pathogens to both humans and animals. Given the limited understanding of transovarial transmission of Anaplasma spp., our study aimed to assess the prevalence of questing larval ticks containing Anaplasma DNA. Additionally, we aimed to gather data for establishing a nationwide forecasting and alert system on seasonal variation of tick developmental stages and tick-borne zoonotic pathogens. Methods From March to October 2021 and again from March to October 2022, we collected a total of 36,912 unfed, questing ticks of Haemaphysalis spp. from 149 sites in South Korea. Ticks were collected from herbaceous vegetation using the flagging method using a white flannel cloth. After species identification, one-third of collected ticks underwent analysis for Anaplasma DNA. Nymph ticks were pooled in groups of 1–10 and larvae in groups of 1–50, while adults were examined individually. Nested polymerase chain reaction (PCR) was performed to detect the genus Anaplasma by amplifying the 16S rRNA gene, followed by sequencing for species identification and phylogenetic analysis. Results Of the 36,912 questing ticks collected, 13,082 (35.4%) were identified as nymphs and adults of H. longicornis and 3850 (10.4%) as those of Haemaphysalis flava. The morphologically indistinguishable larval stage of Haemaphysalis spp. predominated, with 19,980 (54.1%) collected primarily from July to October. From the 939 tick pools, 24 pools (2.6%) tested positive for Anaplasma, with the larval stage exhibiting the highest number of positive pools (16, 1.7%). Phylogenetic analysis revealed that 21 of the 24 Anaplasma-positive pools contained A. phagocytophilum-specific genes, with 1 identified as Anaplasma sp. and the remaining 2 as A. bovis. Conclusions Our study provides evidence of transovarial transmission of A. phagocytophilum in Haemaphysalis spp. larvae under field conditions, showing that the bacteria are transmitted from mother ticks to unengorged, questing larvae. Additionally, our findings contribute significant data for establishing a nationwide forecasting and alert system on seasonal variation of tick developmental stages and tick-borne zoonotic pathogens. Graphical Abstracthttps://doi.org/10.1186/s13071-024-06649-zHaemaphysalis longicornisAnaplasma phagocytophilumTransovarial transmissionLarvaeEpidemiologyTick-borne diseases
spellingShingle KyuSung Ahn
Badriah Alkathiri
Seung-Hun Lee
Haeseung Lee
Dongmi Kwak
Yun Sang Cho
Hyang-Sim Lee
SoYoun Youn
Mi-Sun Yoo
Jaemyung Kim
SungShik Shin
Molecular detection of Anaplasma phagocytophilum in field-collected Haemaphysalis larvae in the Republic of Korea
Parasites & Vectors
Haemaphysalis longicornis
Anaplasma phagocytophilum
Transovarial transmission
Larvae
Epidemiology
Tick-borne diseases
title Molecular detection of Anaplasma phagocytophilum in field-collected Haemaphysalis larvae in the Republic of Korea
title_full Molecular detection of Anaplasma phagocytophilum in field-collected Haemaphysalis larvae in the Republic of Korea
title_fullStr Molecular detection of Anaplasma phagocytophilum in field-collected Haemaphysalis larvae in the Republic of Korea
title_full_unstemmed Molecular detection of Anaplasma phagocytophilum in field-collected Haemaphysalis larvae in the Republic of Korea
title_short Molecular detection of Anaplasma phagocytophilum in field-collected Haemaphysalis larvae in the Republic of Korea
title_sort molecular detection of anaplasma phagocytophilum in field collected haemaphysalis larvae in the republic of korea
topic Haemaphysalis longicornis
Anaplasma phagocytophilum
Transovarial transmission
Larvae
Epidemiology
Tick-borne diseases
url https://doi.org/10.1186/s13071-024-06649-z
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