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. 2021 Mar 25;21(4):242–246. doi: 10.1089/vbz.2020.2716

Prevalence of Borrelia burgdorferi and Anaplasma phagocytophilum in Ixodid Ticks from Southeastern Ukraine

Nadia Kovryha 1, Ala Tsyhankova 1, Olena Zelenuchina 1, Olexandr Mashchak 1, Roman Terekhov 1, Artem S Rogovskyy 2,✉
PMCID: PMC7997714  PMID: 33475465

Abstract

Objectives: Tick-borne diseases have emerged as an increasing medical problem in the world. Being the most prevalent ixodid ticks in Europe, Ixodes ricinus and Dermacentor reticulatus are responsible for transmission of numerous zoonotic pathogens (e.g., human granulocytic anaplasmosis and Lyme borreliosis). Despite their public health significance, studies on the prevalence of tick-borne agents are scare for Eastern Europe. The objective of this study was to examine the prevalence of Anaplasma phagocytophilum, Ehrlichia chaffeensis, and Borrelia burgdorferi sensu lato (B. burgdorferi s. l.) in ixodid ticks from Southeastern Ukraine.

Methods: Over a 5-year period (2014–2018), 358 questing and 389 engorged ixodid ticks were collected from Southeastern Ukraine (Zaporizhzhya region). The ticks were identified as Dermacentor marginatus, D. reticulatus, I. ricinus, and Rhipicephalus rossicus. Nucleic acid samples extracted from tick pools were subjected to RT-PCR analyses for A. phagocytophilum, E. chaffeensis, and B. burgdorferi s. l.

Results: The examined ixodid ticks tested negative for the aforementioned pathogens with the exception of I. ricinus ticks. For questing I. ricinus ticks, minimum infection rates of A. phagocytophilum and B. burgdorferi s. l. were, respectively, 4.2–7.7% and 8.6–12.7%.

Conclusions: These findings will be valuable for medical and veterinary practitioners when risks associated with tick-borne diseases are assessed for southeastern regions of Ukraine.

Keywords: ticks, Anaplasma phagocytophilum, Borrelia burgdorferi s. l, Ehrlichia chaffeensis, Lyme borreliosis, Ukraine

Introduction

To date, vector-borne diseases represent a health problem of increasing significance in the world. Ticks are the leading vectors of human and animal vector-borne diseases (Boulanger et al. 2019). In Europe, including Ukraine, Ixodes ricinus (Linnaeus, 1758) and Dermacentor reticulatus (Fabricius, 1794) are the most prevalent ixodid ticks (Acari: Ixodidae) (Akimov and Nebogatkin 1997, Rubel et al. 2016). I. ricinus ticks are the competent vector for such zoonotic agents as Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato (B. burgdorferi s. l.) among others (Boulanger et al. 2019). In addition to being the proven main vector for some of Babesia spp. and Rickettsia spp., D. reticulatus ticks can also harbor other zoonotic agents (e.g., A. phagocytophilum) (Rubel et al. 2016). Despite the medical importance of the tick-borne diseases (Jahfari et al. 2014, Boulanger et al. 2019, Riccardi et al. 2019, Vandekerckhove et al. 2019, Rogovskyy et al. 2020, Yurchenko et al. 2020), very few studies have examined the prevalence of the aforementioned pathogens in Eastern Europe, specifically Ukraine. Currently, there are no data on the prevalence of zoonotic agents in ticks from any southern or eastern parts of Ukraine. Therefore, the objective of this study was to examine ixodid ticks collected from Southeastern Ukraine for the presence of A. phagocytophilum, Ehrlichia chaffeensis, and B. burgdorferi s. l.

Materials and Methods

A total of 358 questing ixodid ticks were collected through flagging over a 5-year period (2014–2018) at several sites of Zaporizhzhya oblast (region): the City of Berdiansk, Cosmic microdistrict, Khortytsia island, Ridge Canal (Domaha), Velykyi Luh, Zaporizkyi district, Vilnianskyi district, and the City of Zaporizhzhya. Based on their morphology (Filippova 1977), the questing ticks were identified as Dermacentor marginatus (10 females), D. reticulatus (11 females), I. ricinus (220 females, 35 males, and 63 nymphs; in a total of 318 ticks), and Rhipicephalus rossicus (19 females). During the 5-year period, a total of 389 engorged ticks of the respective tick species were obtained from the Zaporizhzhya Oblast Laboratory Center of the Ministry of Health of Ukraine. Of the 389 ticks, 237 engorged ticks, which included 1 D. marginatus tick (1 female), 6 D. reticulatus ticks (5 females and 1 male), 209 I. ricinus ticks (123 females, 14 males, and 72 nymphs), and 21 Rh. rossicus ticks (13 females, 2 males, and 6 nymphs), were collected from humans. The other 152 engorged ticks, which comprised 8 D. marginatus ticks (8 females), 16 D. reticulatus ticks (10 females, 1 male, and 5 nymphs), 110 I. ricinus ticks (94 females, 11 males, and 5 nymphs), and 18 Rh. rossicus ticks (14 females and 4 males), were originated from other animals (Table 1). Of the 152 ticks, 8 D. marginatus ticks were collected from a dog (2 females) and 4 cattle (6 females); 16 D. reticulatus ticks were collected from 3 dogs (2 females and 1 male) and 5 cattle (8 females and 5 nymphs); 110 I. ricinus ticks were collected from 20 dogs (77 females, 11 males, and 5 nymphs), 3 cattle (15 females), and a cat (2 females); and 18 Rh. rossicus ticks were collected from 2 dogs (1 female and 4 males) and 3 cattle (13 females). The collected ticks were immersed in 70% ethanol and stored at 4°C until analyses.

Table 1.

The Prevalence of Anaplasma phagocytophilum, Borrelia burgdorferi Sensu Lato, and Ehrlichia chaffeensis in Ixodid Ticks Collected from Vegetation, Humans, and Other Animals

Pathogens Pools of ticks collected from
 Total
Vegetation
 Humans
 Other animals
 Total by tick stage
F M N F M N F M N F M N
Ixodes ricinus
 A. phagocytophilum 10/32 (172)a 2/4 (26) 2/7 (48) 5/62 (83) 0/4 (4) 2/30 (43) 2/13 (64) 0/2 (11) 0/1 (1) 17/107 (319) 2/10 (41) 4/38 (92) 23/155 (452)
 B. burgdorferi s. l. 27/39 (220) 3/5 (35) 8/11 (63) 21/102 (123) 0/14 (14) 15/58 (72) 6/20 (94) 0/2 (11) 2/3 (5) 54/161 (437) 3/21 (60) 25/72 (140) 82/254 (637)
 E. chaffeensis 0/32 (172) 0/4 (26) 0/7 (48) 0/62 (83) 0/4 (4) 0/30 (43) 0/13 (64) 0/2 (11) 0/1 (1) 0/107 (319) 0/10 (41) 0/38 (92) 0/155 (452)
Dermacentor marginatus
 A. phagocytophilum 0/5 (10) n/a n/a 0/1 (1) n/a n/a 0/5 (8) n/a n/a 0/11 (19) n/a n/a 0/11 (19)
 E. chaffeensis 0/5 (10) n/a n/a 0/1 (1) n/a n/a 0/5 (8) n/a n/a 0/11 (19) n/a n/a 0/11 (19)
Dermacentor reticulatus
 A. phagocytophilum 0/7 (11) n/a n/a 0/5 (5) 0/1 (1) n/a 0/5 (10) 0/1 (1) 0/2 (5) 0/17 (26) 0/2 (2) 0/2 (5) 0/21 (33)
 E. chaffeensis 0/7 (11) n/a n/a 0/5 (5) 0/1 (1) n/a 0/5 (10) 0/1 (1) 0/2 (5) 0/17 (26) 0/2 (2) 0/2 (5) 0/21 (33)
Rhipicephalus rossicus
 A. phagocytophilum 0/5 (19) n/a n/a 0/12 (13) 0/2 (2) 0/5 (6) 0/4 (14) 0/1 (4) n/a 0/21 (46) 0/3 (6) 0/5 (6) 0/29 (58)
 E. chaffeensis 0/5 (19) n/a n/a 0/12 (13) 0/2 (2) 0/5 (6) 0/4 (14) 0/1 (4) n/a 0/21 (46) 0/3 (6) 0/5 (6) 0/29 (58)
Open in a new tab
a

Values correspond to number of PCR-positive tick pools/total numbers of tick pools tested. In the parentheses are indicated the total number of individual ticks tested per a total number of pools.

F, female; M, male; N, nymphal ticks; n/a, nonapplicable.

Nucleic acid (DNA and RNA) was extracted from pooled ticks (1–10 ticks per pool). For that, commercially available nucleic acid extractions kits, “RIBO-Prep” (AmpliPrime) and “RealBest Extraction 100” (Vector-Best) were used. DNA isolation control was also used according to the manufacturers' instructions. All the samples were then subjected to a multiplex RT-PCR. The pools were tested through “AmpliSens TBEV, B. burgdorferi s. l., A. phagocytophilum, E. chaffeensis/E. muris-F” and/or “RealBest DNA Borrelia burgdorferi s. l.” (Central Research Institute for Epidemiology) by using the iCycler iQ5 thermocycler (BioRad Laboratories) according to the manufacturers' instructions. Pools of I. ricinus, D. marginatus, D. reticulatus, or Rh. rossicus ticks were examined for the presence of A. phagocytophilum and E. chaffeensis. I. ricinus ticks were also analyzed for B. burgdorferi s. l. The numbers of ticks and their pools tested are provided in Table 1. Where applicable, minimum infection rates (%) of A. phagocytophilum and B. burgdorferi s. l. were calculated for I. ricinus ticks with the assumption that only one tick in each positive pool was infected (no. of ticks tested/minimal no. infected; Table 2). Importantly, the internal positive and negative controls provided by the kits were included in each PCR reaction. No approval from institutional ethics committee was required for this study.

Table 2.

The Minimum Infection Rates of Anaplasma phagocytophilum and Borrelia burgdorferi Sensu Lato in Ixodes ricinus Ticks

Pathogens Pools of ticks collected from
Vegetation
 Humans
 Other animals
 Total by tick stage
F M N F M N F M N F M N
A. phagocytophilum 5.8a 7.7 4.2 6.0 n/a 4.7 3.1 n/a n/a 5.3 4.9 4.3
B. burgdorferi s. l. 12.3 8.6 12.7 17.1 n/a 20.8 6.4 n/a 40.0 12.3 5.0 17.9
Open in a new tab
a

Values correspond to minimum infection rates (%), which were calculated with the assumption that only one tick in each positive pool was infected (no. of ticks tested/minimal no. infected).

Results

The PCR results showed that all the analyzed pools of D. marginatus (n = 11), D. reticulatus (n = 21), and Rh. rossicus (n = 29) ticks were negative for A. phagocytophilum and E. chaffeensis (Table 1). Furthermore, all the pools of I. ricinus ticks (n = 155) tested negative for E. chaffeensis as well. In contrast, a total of 14.8% (23 PCR-positive pools out of 155 pools tested; 23/155) pools of questing and engorged I. ricinus adults were positive for A. phagocytophilum. The highest proportions of A. phagocytophilum-positive pools were detected for questing I. ricinus adults (33.3%; 12/36) followed by 13.3% (2/15) and 7.6% (5/66) of engorged I. ricinus adults collected from animals and humans, respectively. In addition, a total of 4 pools of questing (2/7) and engorged I. ricinus nymphs (2/31) were PCR-positive for A. phagocytophilum (Table 1). The calculated minimum infection rates of I. ricinus ticks for A. phagocytophilum are provided in Table 2.

Besides the two tick-borne pathogens tested, some pools of I. ricinus adults and nymphs were also examined for the presence of B. burgdorferi s. l. The results demonstrated that a total of 32.3% of pools of both questing and engorged I. ricinus ticks carried B. burgdorferi s. l. DNA (Table 1). The highest percentage of positive pools of I. ricinus ticks were observed for questing nymphs (72.7%; 8/11) and adults (68.2%; 30/44). Furthermore, 18.1% pools of engorged adults (21/116) and 25.9% pools of engorged nymphs (15/58) collected from humans were PCR-positive for B. burgdorferi s. l. Finally, 27.3% (6/22) and 66.7% (2/3) pools of engorged adults and nymphs of I. ricinus collected from animals tested positive for B. burgdorferi s. l. DNA (Table 1). The minimum infection rates of questing I. ricinus ticks for B. burgdorferi s. l. were 12.3%, 8.6%, and 12.7% for females, males, and nymphs, respectively (Table 2).

Discussion

This study demonstrated that, in Southeastern Ukraine (Zaporizhzhya region), the minimum infection rates of A. phagocytophilum for I. ricinus ticks varied from 3.1% for engorged females and 4.2% for questing nymphs to 6.0% for engorged females and 7.7% for questing males (Table 2). These rates were comparable with the infection rates of A. phagocytophilum, which were previously recorded for individually tested questing I. ricinus ticks collected in Eastern Ukraine (3.6%), Central Ukraine (2.7–5.2%), and Northern Ukraine (0.4%) (Movila et al. 2009, Didyk et al. 2017, Rogovskyy et al. 2017, 2018, 2019). Similar to Ukraine, low infection rates of A. phagocytophilum were reported in questing I. ricinus ticks from neighboring countries such as Belarus (4.2%), Lithuania (2.9%), Moldova (5.1–9.0%), Poland (10.7%), Russia (3.1%), and Slovakia (5.5%) (Grzeszczuk et al. 2004, Koci et al. 2007, Radzijevskaja et al. 2008, Movila et al. 2009, Pangracova et al. 2013, Reye et al. 2013, Kiewra et al. 2014, Livanova et al. 2018).

This investigation did not identify A. phagocytophilum DNA in D. marginatus and D. reticulatus ticks. The lack of detection could be explained by low numbers of ticks analyzed and an overall low infection rate of this pathogen in Dermacentor ticks reported for Ukraine in the past (Movila et al. 2009, Didyk et al. 2017, Rogovskyy et al. 2017, 2018, 2019). Recent study showed that only 1.0% of questing D. reticulatus ticks (a total of 98 individual ticks analyzed; n = 98) from Central Ukraine (Kyiv) carried A. phagocytophilum DNA (Rogovskyy et al. 2018). Moreover, all individually analyzed ticks of D. reticulatus collected from Northern Ukraine (n = 100) and neighboring Belarus (n = 164) were consistently PCR-negative for A. phagocytophilum (Reye et al. 2013, Rogovskyy et al. 2019). In addition to A. phagocytophilum, the ticks were also examined for another member of the Anaplasmataceae family, E. chaffeensis, the causative agent of human monocytic ehrlichiosis, which is extremely rare in Europe (Yabsley 2010). Expectedly, this study did not detect E. chaffeensis DNA in the examined ticks.

Rh. rossicus (Jakimov et Kohl-Jakimova, 1911) and infection rates of various pathogens for this vector are highly understudied. This tick species is known to have a vectoral role for only a few pathogens (Francisella tularensis, Crimean-Congo hemorrhagic fever virus, and West Nile virus) and, for most European countries, Rh. rossicus (Jakimov et Kohl-Jakimova, 1911) is considered an alien tick (Mihalca et al. 2015). Rh. rossicus is indigenous to Ukraine. Recently, the habitat of Rh. rossicus was considerably expanded from the south to the north of Ukraine (Mihalca et al. 2015). This study demonstrated that all the examined Rh. rossicus ticks tested negative.

Although Lyme borreliosis (LB) has been steadily on the rise in Ukraine (Carriveau et al. 2019, Rogovskyy et al. 2020), very few studies have investigated prevalence of B. burgdorferi s. l. in ixodid ticks from this country (Movila et al. 2009, Didyk et al. 2017, Rogovskyy et al. 2017, 2018, 2019). Furthermore, the published epidemiological data were generated only for Central and Western Ukraine (Movila et al. 2009, Didyk et al. 2017, Rogovskyy et al. 2017, 2018, 2019, Weiner et al. 2018). Thus, this study examined the prevalence of B. burgdorferi s. l. in I. ricinus ticks from Southeastern Ukraine. The results demonstrated that the minimum infection rates of B. burgdorferi s. l. in questing I. ricinus ticks were 12.3%, 8.6%, and 12.7% for females, males, and nymphs, respectively (Table 2). Overall, these rates are consistent with the findings of previous studies, where 4.4% and 5.2–13.5% of individually analyzed ticks from Western (Ternopyl region) and Central (Kyiv and the CEZ) Ukraine were found to carry B. burgdorferi s. l. DNA (Didyk et al. 2017, Rogovskyy et al. 2018, 2019, Weiner et al. 2018).

Conclusions

This study is the first to investigate the prevalence of A. phagocytophilum, B. burgdorferi, and E. chaffeensis in ixodid ticks collected from Southeastern Ukraine. Pools of I. ricinus, D. marginatus, D. reticulatus, or Rh. rossicus were examined for the presence of A. phagocytophilum and E. chaffeensis by PCR. The data demonstrated that all the ticks were consistently negative for the two pathogens with the exception of I. ricinus ticks, which tested positive for A. phagocytophilum. Moreover, I. ricinus ticks were also analyzed for B. burgdorferi s. l. The result demonstrated that 12.3%, 8.6%, and 12.7% of females, males, and nymphs, respectively, tested positive for B. burgdorferi s. l. The newly provided data should be highly valuable for both medical and veterinary practitioners as well as epidemiologists when assessing the risks associated with tick-borne diseases for Southeastern Ukraine.

Acknowledgments

The authors thank the U.S. Department of Defense, Defense Threat Reduction Agency (DTRA), and Biological Threat Reduction Program (BTRP) for their assistance in publication of this article. Although DTRA/BTRP did not support the research described in this publication, the program supported the article development and publication. The contents of this publication are the responsibility of the authors and do not necessarily reflect the views of DTRA or the U.S. Government.

Author Disclosure Statement

No conflicting financial interests exist.

Funding Information

This study was supported by the Ministry of Health of Ukraine (Ukraine) and Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University (United States). Importantly, the authors acknowledge the financial support of U.S. Department of Defense, Defense Threat Reduction Agency (DTRA), and Biological Threat Reduction Program (BTRP) in publication of this article.

References

  1. Akimov IA, Nebogatkin IV. Ixodid ticks (Acari, Ixodidae) specific composition of Ukraine. Vestnik Zoologii 1997; 31:75–77 [Google Scholar]
  2. Boulanger N, Boyer P, Talagrand-Reboul E, Hansmann Y. Ticks and tick-borne diseases. Med Mal Infect 2019; 49:87–97 [DOI] [PubMed] [Google Scholar]
  3. Carriveau A, Poole H, Thomas A. Lyme disease. Nurs Clin North Am 2019; 54:261–275 [DOI] [PubMed] [Google Scholar]
  4. Didyk YM, Blanarova L, Pogrebnyak S, Akimov I, et al. Emergence of tick-borne pathogens (Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Ricketsia raoultii and Babesia microti) in the Kyiv urban parks, Ukraine. Ticks Tick Borne Dis 2017; 8:219–225 [DOI] [PubMed] [Google Scholar]
  5. Filippova NA. Ixodid ticks of the subfamily Ixodinae. Fauna of the USSR. Arachnida. Leningrad: Publishing House Nauka, 1977 [Google Scholar]
  6. Grzeszczuk A, Ziarko S, Prokopowicz D, Radziwon PM. Infection of bison from the Belovezhska pushcha with Anaplasma phagocytophilum. Med Wet 2004; 37:29–38 [Google Scholar]
  7. Jahfari S, Coipan EC, Fonville M, van Leeuwen AD, et al. Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasit Vectors 2014; 7:365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kiewra D, Zalesny G, Czulowska A. The prevalence of Anaplasma phagocytophilum in questing Ixodes ricinus ticks in SW Poland. Pol J Microbiol 2014; 63:89–93 [PubMed] [Google Scholar]
  9. Koci J, Movila A, Taragel'ova V, Toderas I, et al. First report of Anaplasma phagocytophilum and its co-infections with Borrelia burgdorferi sensu lato in Ixodes ricinus ticks (Acari: Ixodidae) from Republic of Moldova. Exp Appl Acarol 2007; 41:147–152 [DOI] [PubMed] [Google Scholar]
  10. Livanova NN, Fomenko NV, Akimov IA, Ivanov MJ, et al. Dog survey in Russian veterinary hospitals: tick identification and molecular detection of tick-borne pathogens. Parasit Vectors 2018; 11:591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Mihalca AD, Kalmar Z, Dumitrache MO. Rhipicephalus rossicus, a neglected tick at the margin of Europe: a review of its distribution, ecology and medical importance. Med Vet Entomol 2015; 29:215–224 [DOI] [PubMed] [Google Scholar]
  12. Movila A, Rolain JM, Podavalenko A, Toderas I, et al. Detection of spotted fever group rickettsiae and family Anaplasmataceae in Ixodes ricinus ticks from Republic of Moldova and Eastern Ukraine. Clin Microbiol Infect 2009; 15(Suppl 2):32–33 [DOI] [PubMed] [Google Scholar]
  13. Pangracova L, Derdakova M, Pekarik L, Hviscova I, et al. Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia. Parasit Vectors 2013; 6:238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Radzijevskaja J, Paulauskas A, Rosef O. Prevalence of Anaplasma phagocytophilum and Babesia divergens in Ixodes ricinus ticks from Lithuania and Norway. Int J Med Microbiol 2008; 298:218–221 [Google Scholar]
  15. Reye AL, Stegniy V, Mishaeva NP, Velhin S, et al. Prevalence of tick-borne pathogens in Ixodes ricinus and Dermacentor reticulatus ticks from different geographical locations in Belarus. PLoS One 2013; 8:e54476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Riccardi N, Antonello RM, Luzzati R, Zajkowska J, et al. Tick-borne encephalitis in Europe: a brief update on epidemiology, diagnosis, prevention, and treatment. Eur J Intern Med 2019; 62:1–6 [DOI] [PubMed] [Google Scholar]
  17. Rogovskyy A, Batool M, Gillis DC, Holman PJ, et al. Diversity of Borrelia spirochetes and other zoonotic agents in ticks from Kyiv, Ukraine. Ticks Tick Borne Dis 2018; 9:404–409 [DOI] [PubMed] [Google Scholar]
  18. Rogovskyy AS, Biatov AP, Davis MA, Liu S, et al. Upsurge of Lyme borreliosis in Ukraine: a 20-year survey. J Travel Med 2020;27:1–3 [DOI] [PubMed] [Google Scholar]
  19. Rogovskyy AS, Nebogatkin IV, Scoles GA. Ixodid ticks in the megapolis of Kyiv, Ukraine. Ticks Tick Borne Dis 2017; 8:99–102 [DOI] [PubMed] [Google Scholar]
  20. Rogovskyy AS, Threadgill DW, Akimov IA, Nebogatkin IV, et al. Borrelia and other zoonotic pathogens in Ixodes ricinus and Dermacentor reticulatus ticks collected from the Chernobyl exclusion zone on the 30th Anniversary of the nuclear disaster. Vector Borne Zoonotic Dis 2019; 19:466–473 [DOI] [PubMed] [Google Scholar]
  21. Rubel F, Brugger K, Pfeffer M, Chitimia-Dobler L, et al. Geographical distribution of Dermacentor marginatus and Dermacentor reticulatus in Europe. Ticks Tick Borne Dis 2016; 7:224–233 [DOI] [PubMed] [Google Scholar]
  22. Vandekerckhove O, De Buck E, Van Wijngaerden E.. Lyme disease in Western Europe: an emerging problem? A systematic review. Acta Clin Belg 2019. [Epub ahead of print]; DOI: 10.1080/17843286.2019.1694293 [DOI] [PubMed] [Google Scholar]
  23. Weiner M, Zukiewicz-Sobczak W, Tokarska-Rodak M, Plewik D, et al. Prevalence of Borrelia burgdorferi sensu lato in ticks from the Ternopil region in Ukraine. J Vet Res 2018; 62:275–280 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Yabsley MJ. Natural history of Ehrlichia chaffeensis: vertebrate hosts and tick vectors from the United States and evidence for endemic transmission in other countries. Vet Parasitol 2010; 167:136–148 [DOI] [PubMed] [Google Scholar]
  25. Yurchenko OO, Dubyna DO, Vynograd NO, Rogovskyy AS. Tick-borne encephalitis cases recorded in Ukraine over 1990–2018. J Travel Med 2020;27:taaa075. [DOI] [PMC free article] [PubMed] [Google Scholar]

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