Transovarial transmission of Anaplasma phagocytophilum in Haemaphysalis ticks under field conditions

doi:10.21203/rs.3.rs-5275154/v1

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Transovarial transmission of Anaplasma phagocytophilum in Haemaphysalis ticks under field conditions

https://doi.org/10.21203/rs.3.rs-5275154/v1

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Background:

Anaplasmosis, a zoonotic tick-borne pathogen affecting both livestock, companion animals, and humans, exhibits 15 to 18% seropositivity among hunting dogs in Korea. The dominant tick species in Korea, Haemaphysalis longicornis can transmit this pathogen 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 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 gene. Nymph ticks were pooled in groups of one to 10, larvae in groups of one to 50, while adults were examined individually. Nested 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 3,850 (10.4%) as those of H. flava. The morphologically indistinguishable larval stage of Haemaphysalis 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, while the remaining 1 was identified as Anaplasma sp. and 2 as A. bovis.

Conclusions:

Our study provides evidence of transovarial transmission of Anaplasma phagocytophilum in Haemaphysalis spp. larvae under field conditions, as A. phagocytophilum originates from their mother ticks in unengorged questing larval ticks. 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.

Haemaphysalis longicornis

Anaplasma phagocytophilum

transovarial transmission

larvae

epidemiology

tick-borne diseases

The longhorned bush tick, Haemaphysalis longicornis, is native to eastern Asian countries, including Korea, Japan, and China. It has also established populations in Australia, New Zealand, several Pacific islands, and recently in the eastern United States [1]. Haemaphysalis longicornis is the predominant tick species found in both wild and domestic animals, as well as in humans in Korea, followed by H. flava [2, 3, 4, 5]. These two tick species are known to host and transmit a variety of pathogens, including Anaplasma phagocytophilum, A. bovis, A. platys, Ehrlichia chaffeensis, Francisella tularensis, Bartonella henselae, B. quintana, Rickettsia japonica, R. rickettsii, Tick-borne Encephalitis Virus, Severe Fever with Thrombocytopenia Syndrome Virus (SFTSV), and a number of Babesia and Theileria species in Korea [6, 7].

Among tick-borne pathogens, A. phagocytophilum is a particularly significant zoonotic pathogen, which infects granulocytic white blood cells in mammalian hosts and causes human granulocytic anaplasmosis [6]. A serological survey indicates that 15.6–18.8% of outdoor dogs are exposed to this pathogen in Korea [8, 9]. Anaplasma phagocytophilum causes an acute febrile illness in dogs, characterized by lethargy and inappetence [10]. Less frequent signs in dogs include lameness, coughing, polydipsia, intermittent vomiting, and hemorrhages. Pathogens such as A. phagocytophilum in unfed larval ticks are inherited from their female mother tick through the transovarial route in Ixodes ricinus [11]. The larval stage of Haemaphysalis spp. measures only 0.58–0.62 mm in length and 0.47–0.51 mm in breadth [12], and they quest in large numbers near their hatching sites. Consequently, infestations with larval ticks often go unnoticed, while simultaneously exposing hosts to a variety of tick-borne pathogens.

This study focuses on the occurrence of A. phagocytophilum in Haemaphysalis ticks, with particular interest in the questing larval stage. Ticks were collected from four southwestern provinces of Korea, and Anaplasma-positive Haemaphysalis ticks were identified and analyzed.

Tick collection

Unfed, questing ticks were collected from herbaceous vegetation using the flagging method, employing a white flannel cloth measuring 100 x 100 cm. Ticks were collected from 149 sites across the four southwestern and central provinces of the Republic of Korea between March and October 2021, and again from March to October 2022 (Fig. 1). The collection sites were located in the Jeonnam, Jeonbuk, Chungnam, and Chungbuk regions, with Daejeon Metropolitan City and Sejong Special Self-Governing City included in the Chungnam region, and Gwangju Metropolitan City included in the Jeonnam region. This study was conducted as part of a pioneering project before an annual nationwide surveillance program for tick and tick-borne diseases is launched. The study regions included areas where 18.8% of outdoor dogs tested serologically positive for A. phagocytophilum [9]. Collected ticks were preserved in 70% ethanol, and their developmental stages and species were identified based on morphological characteristics, using a stereo microscope and taxonomic key [13].

After species identification, ticks were pooled by species, developmental stage, survey period, and collection site. Adults and nymphs were identified to the species level, whereas larvae were identified to the genus level due to morphological similarities among species [13]. The number of ticks per pool ranged from one to ten for nymphs and one to fifty for larvae, while adults were individually examined.

DNA Extraction and PCR detection

Genomic DNA was extracted using a DNeasy Blood & Tissue Kit (Qiagen, Hilden, Germany) following the manufacturer’s instructions. PCR was performed using an AccuPower HotStart PCR Premix Kit (Bioneer, Daejeon, Republic of Korea). Nested PCR was conducted to detect the genus Anaplasma by amplifying the 16S rRNA gene, as previously described [14], using the primer pairs EE1/EE2 and EE3/EE4, which generated an amplicon of 924–926 bp. A sample of A. phagocytophilum detected in cattle in the Republic of Korea [15] served as a positive control, while a sample without a DNA template was used as a negative control. The minimum infection rate (MIR) of pooled ticks with Anaplasma spp. was calculated using the following equation: (number of positive pools of ticks / total number of ticks tested) × 100.

Sequencing and Phylogenetic Analyses

All PCR-positive products with EE3/EE4 primers were sent to Macrogen (Daejeon, Republic of Korea) for Sanger sequencing. The obtained sequences, along with those previously reported in GenBank, were aligned and analyzed using the multiple sequence alignment program CLUSTAL Omega (v. 1.2.1, Bioweb, Ferndale, WA, USA). Unnecessary sequences at the front and back ends were trimmed based on the sequences detected in this study, using BioEdit (v. 7.2.5, Bioedit, Manchester, UK). Sites containing gaps or ambiguous alignment were removed before phylogenetic analysis. Phylogenetic analysis was conducted using the maximum likelihood method with the Kimura two-parameter distance model in molecular evolutionary genetics analysis [16]. The aligned sequences of Anaplasma 16S rRNA were pairwise compared to determine homology, and the stability of the obtained trees was estimated using bootstrap analysis with 1,000 replicates.

For the estimation of evolutionary divergence between sequences of Anaplasma spp. identified in this study, analyses were conducted using the Maximum Composite Likelihood model [17]. This analysis involved 25 nucleotide sequences, and all ambiguous positions were removed for each sequence pair (pairwise deletion option). There was a total of 881 positions in the final dataset. Evolutionary analyses were conducted in MEGA11 [16].

A total of 36,912 questing ticks of the genus Haemaphysalis were collected from 149 sites (Table 1). The distribution of ticks was as follows: 12,869 from Jeonnam, 5,899 from Jeonbuk, 10,584 from Chungnam, and 8,560 from Chungbuk provinces. Among these, larvae represented the highest proportion among the three developmental stages (19,980 ticks, 54.1%), while adults made up the lowest (1,434 ticks, 3.9%). However, species identification of larvae was not recorded due to the morphological indistinguishability between the larval stages of H. longicornis and H. flava.

Nymph and adult stages of H. longicornis (13,082 ticks, 35.4%) and H. flava (3,850 ticks, 10.4%) were collected from all four provinces, with H. longicornis being the dominant species. The occurrence of H. longicornis nymphs and adults was primarily observed from April to July, with peak occurrences in May for nymphs and July for adults, respectively. In contrast, the occurrence of H. flava nymphs and adults was observed from March to June, with peak occurrence in March for both nymphs and adults (Additional file 1: Table S1).

Table 1. Number of Haemaphysalis tick species collected from the study area

The monthly occurrence of Haemaphysalis ticks by developmental stages from March to October is illustrated in Fig. 2, with a detailed breakdown presented in Additional file 1: Table S1. From March to July, the nymphal stage dominated the study areas, with 94.9% of the nymphal ticks collected during this period, peaking in April. Conversely, the larval stage was predominantly collected from July to October, accounting for 92.9% of the larvae collected during these months, with the highest peak observed in September. The collection of adult stages was comparatively low (1,434 ticks, 3.9%) compared to the larval (19,980 ticks, 54.1%) and nymphal (15,498 ticks, 42.0%) stages, with the highest number of adults collected in July (451 ticks, 1.3%).

Of the ticks collected, approximately one-third (13,118 ticks, 35.5%) underwent PCR analysis to detect Anaplasma infection. They were pooled into 939 groups, which were then subjected to PCR analysis followed by sequencing for species identification and phylogenetic analysis. Out of the 939 pools of ticks, 24 pools (2.6%) tested positive for Anaplasma. The larval stage exhibited the highest number of Anaplasma-positive pools (16 pools, 1.7%), followed by the nymphal (7 pools, 0.7%) and adult (1 pool, 0.1%) stages (Table 2).

Anaplasma-positive pools were found in the nymphal and adult stages of H. longicornis, but none of the H. flava pools contained Anaplasma-specific DNA. The minimum infection rate (MIR) of Anaplasma from the 13,118 ticks was calculated to be 0.183%. High numbers of Anaplasma-positive pools were observed in Chungnam and Chungbuk provinces, each with 9 positive pools, while Jeonnam and Jeonbuk provinces had 5 and 1 positive pools, respectively.

The monthly occurrence of Anaplasma-positive pools is depicted in Fig. 3. The pattern of Anaplasma-positive pools coincided with the monthly occurrence of Haemaphysalis tick stages. Positive pools in the nymphal stage were found from April to July, while Anaplasma-positive larval pools were observed from August to October. One positive pool in the adult stage was found in July, coinciding with the peak occurrence of adult ticks. The highest peak occurrence of Anaplasma-positive pools was observed in September, which corresponded with the peak in larval tick activity.

Table 2 Souce of Anaplasma-positive tick pools of Haemaphysalis spp. in Korea

¹MIR, minimum infection rate (number of positive pools of ticks / total number of ticks tested × 100); ² MIR within each developmental stage of tick

Phylogenetic analysis of the PCR-positive pools for Anaplasma spp. revealed that 21 of the 24 Anaplasma-positive pools contained A. phagocytophilum-specific gene, while the remaining 2 and 1 were identified as A. bovis and Anaplasma sp., respectively (Fig. 4). The two A. bovis sequences were found in a pool of H. longicornis nymphs collected in Sejong-si in June and in an adult male tick collected in Chungnam province in July. Sixteen A. phagocytophilum-positive pools were identified from larval ticks, while six positive pools were from nymphs.

The mean divergence between the sixteen sequences of A. phagocytophilum from the larval stage was 0.0021 ± 0.0048 (Mean ± SD, Max 0.0207, Additional file 1: Table S2). Twenty-one sequences of A. phagocytophilum identified in this study, including all 16 sequences from larval ticks, were grouped together (Fig. 4). The mean divergence of the 24 A. phagocytophilum sequences compared to A. phagocytophilum identified from a Korean water deer was 0.0033 ± 0.0077. Therefore, A. phagocytophilum identified from the 16 larval pools of Haemaphysalis ticks appeared to be highly similar. The 16 larval pools of A. phagocytophilum originated from all four provinces investigated in this study: 5 from Jeonnam, 1 from Jeonbuk, 4 from Chungnam, and 6 from Chungbuk.

Representative sequences obtained from this study and used in the phylogenetic analysis were submitted to the GenBank database (accession numbers: PP663778–PP663807).

Seasonal occurrence of Haemaphysalis ticks in Korea compared to other regions

The survey conducted in the southwestern provinces of South Korea during 2021 and 2022 revealed H. longicornis as the predominant tick species, followed by H. flava. Nymphal ticks were prevalent from March to July, while larval ticks were most commonly collected from July to October, with adult ticks peaking in July. These findings are consistent with previous reports on the seasonal distribution of H. longicornis near the demilitarized zone in Korea and in Virginia, USA [18, 19]. The life cycle of H. longicornis in these regions follows a similar seasonal trend, with adults active in the summer, larvae peaking in the fall, and nymphs overwintering and becoming active in the spring [20, 21, 22]. Given that H. longicornis is associated with large wild and domestic mammals and H. flava with small- to medium-sized mammals and birds [18], Korea's landscape of grass- and herb-covered hills with scattered trees provides an ideal habitat for both species.

Larval ticks as the major source for Anaplasma transmission

Results of this study indicates that the larval stage of Haemaphysalis ticks carried significantly more Anaplasma pathogens than the nymphal or adult stages, as two-thirds of Anaplasma-positive pools were from larval ticks. The high occurrence of Anaplasma-positive larvae likely stems from the large number of larvae collected. The minimum infection rate (MIR) for the larval stage was 0.224, compared to 0.121 for nymphs and 0.592 for adults (Table 2). Although the adult stage had a higher MIR, the large number of larvae and the presence of transovarial transmission of A. phagocytophilum in Haemaphysalis ticks suggest that larval ticks are an important vector for A. phagocytophilum in Korea.

MIR of A. phagocytophilum in different tick stages

The lower MIR in nymphal ticks compared to larval ticks may be influenced by various factors. While a higher number of positive pools in nymphal ticks might be expected due to the cumulative effect of transovarial transmission and additional new infections during blood-feeding in the larval stage, the host preferences of different tick stages and the infection status of A. phagocytophilum in these hosts could affect the infection rates. No A. phagocytophilum-positive adult ticks were detected in this study, though previous studies have found A. phagocytophilum in adult H. longicornis in Korea [23]. The small sample size of adult ticks (169 compared to 7,153 larvae for PCR) may explain this result.

Fall as the larval tick season in Korea

Anaplasma-positive larval ticks were observed from July to October, with a peak in September (Fig. 3). This suggests that public health campaigns in Korea should emphasize the increased risk of Anaplasma transmission during this period, particularly from the tiny, difficult-to-detect larval ticks, which measure only 0.6 mm in length [12]. Scrub typhus, also known as tsutsugamushi disease, is a common febrile vector-borne disease in South Korea caused by an intracellular bacterium, Orientia tsutsugamushi [24]. The disease is transmitted by the chigger, the larval stage of the trombiculid mite, and has a marked seasonality in incidence, peaking in autumn [25]. Anaplasmosis and scrub typhus would therefore better be addressed together during outdoor activities in the autumn season in Korea.

The importance of transovarial transmission for A. phagocytophilum

This study strongly supports the transovarial transmission of A. phagocytophilum from female Haemaphysalis ticks to their larvae, as all collected larvae were questing, unengorged ticks from vegetation rather than host animals. This finding is consistent with studies on Ixodes ricinus in Germany [11] and Dermacentor albipictus in North America [26]. While A. phagocytophilum was the predominant Anaplasma species detected, A. bovis was also found in one nymphal and one adult tick pool, highlighting the veterinary and medical significance of transovarial transmission in tick-borne diseases.

High prevalence of A. phagocytophilum in dogs in Korea and larval tick infestation

The role of larval Haemaphysalis ticks in transmitting Anaplasma to human or animal hosts has not been fully investigated, and there are no reports of clinical cases of anaplasmosis caused by larval ticks in Korea. However, previous studies have reported a relatively high seroprevalence of A. phagocytophilum (15.6–18.8%) among outdoor dogs, including hunting dogs, in Korea [8, 9]. Although no specific data on the contribution of larval ticks to this high seroprevalence were provided, the tiny size of larval Haemaphysalis ticks and their abundant distribution may explain the high infection rates in dogs. One of the authors in this study has created a YouTube video demonstrating the potential dangers of larval tick infestations on dogs in Korea [27].

Forecasting and public awareness campaigns on larval ticks

Given the high prevalence of Anaplasma spp. in questing larval ticks, it appears to be crucial to raise awareness about the risks of tick-borne infections for both animals and humans by larval ticks. Preventive measures should be emphasized, especially for long-haired animals, as larval ticks are difficult to detect. The high tick occurrence throughout the spring-summer-fall seasons, as indicated in Fig. 2, underscores the need for forecasting and monitoring tick populations and pathogens. Public health campaigns, similar to those for mosquito-borne diseases like Japanese encephalitis, should be implemented to mitigate the risk of tick-borne illnesses in Korea [28].

This study provides valuable insights into the prevalence and transmission dynamics of Anaplasma spp. in Haemaphysalis ticks in South Korea. The findings highlight the importance of transovarial transmission in the epidemiology of tick-borne pathogens and underscore the need for proactive measures to mitigate the risk of tick-borne diseases. Additionally, we recommend implementing a nationwide forecasting and alert system to monitor seasonal variations in tick developmental stages and tick-borne zoonotic pathogens such as A. phagocytophilum.

MIR

minimum infection rate

s.l.

sensu lato

TBE

Tick-born encephalitis

Ethics approval and consent to participate
Not applicable. Approval from Chonnam National University’s Institutional Animal Care and Use Committee was not required for the present study, because the collected samples from questing ticks in the environment in this study did not cause hazard to any animals. Ticks are not included in the endangered species of Korea. Specific approval for each collection site was not needed because the sites were not located within national parks or protected regions.

Consent for publication
Not applicable.

Competing interests

The authors declare that they have no competing interests.

Funding

This research was funded by Animal and Plant Quarantine Agency (QIA), Republic of Korea, grant number Z-1543081-2021-22-02.

Author Contribution

KA: Methodology, field work, validation, investigation, formal analysis, writing - original draft. BA, HL: Methodology, field work, validation, SL, DK: Conceptualization, field work, methodology, validation, writing - review and editing. YSC, HL, SY, MY, JK: Conceptualization, validation, review. SS: Conceptualization, validation, writing, visualization, supervision.

Acknowledgement

This paper has been sponsored by Elanco Animal Health in the framework of the CVBD® World Forum Symposium.

Availability of data and materials

The datasets generated and analyzed during the current study are not publicly available due to confidentiality commitment with the Korean government, but are available from the corresponding author on reasonable request.

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Transovarial transmission of Anaplasma phagocytophilum in Haemaphysalis ticks under field conditions

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Abstract

Background:

Methods:

Results:

Conclusions:

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Introduction

Materials and Methods

Results

Discussion

Conclusion

Abbreviations

Declarations

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Not applicable.

Competing interests

Funding

Author Contribution

Acknowledgement

Availability of data and materials

References

Additional Declarations

Supplementary Files

Status:

Version 1

Transovarial transmission of Anaplasma phagocytophilum in Haemaphysalis ticks under field conditions

Status:

Version 1

Abstract

Background:

Methods:

Results:

Conclusions:

Figures

Introduction

Materials and Methods

Results

Discussion

Conclusion

Abbreviations

Declarations

Consent for publication Not applicable.

Competing interests

Funding

Author Contribution

Acknowledgement

Availability of data and materials

References

Additional Declarations

Supplementary Files

Status:

Version 1

Consent for publication
Not applicable.