Diversity and Distribution of Bacterial and Parasitic Tick-Borne Pathogens in Armenia, Transcaucasia
-
Sargis Aghayan
,
Gohar Grigoryan
,
Hasmik Gevorgyan
,
Tehmine Harutyunyan
,
Martin Rukhkyan
,
Vahagn Muradyan
,
Gregory Karadjian
,
Maud Marsot
,
Sara Moutailler
,
Thomas Pollet
Abstract
Background: Variations in the distribution and prevalence of pathogens in ticks can have significant consequences for human health. Information on these variables in Transcaucasia is scarce, so the aim of our study was to conduct a large-scale study to detect selected tick-borne infectious agents in Armenia.
Methods: Overall, 209 adult ticks were collected from different hosts including 4 samples from human clothes. We tested ticks using high-throughput microfluidic single-cell real-time PCR to detect 42 genospecies of pathogens. We used GIS to determine biotic and abiotic factors governing the prevalence of pathogens and applied statistical analyses to test the association between prevalence of pathogens depending on hosts, locality and environment.
Results: From 209 samples, 134 were positive to targeted pathogens. Anaplasma phagocytophilum Foggie, 1949 was the most prevalent case (44%). The highest overall prevalence was observed in ticks from sheep (74%), followed by cows (67%) and calves (60%). The highest multiple infection rates were also detected in sheep (40%) and calves (40%) followed by cows (28%). One statistically significant association was found among co-infections (P<0.05). The prevalence of pathogens varied according to locality. The abundance of Anaplasma spp. is significantly correlated with “slope” and “vegetation” factors. Similar patterns were detected for other pathogens.
Conclusion: This was the first large-scale survey of multiple tick-borne pathogens in Armenia and Transcaucasia. The results of this study shed light on spatial variations in pathogen infection rate among adult ticks found on hosts and underline a number of environmental determinants of pathogen distribution among ticks.
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28. Tarasevit I V, Plotnikova LF, Jablonskaja VA, et al (1976). Natural foci of rick-ettsioses in the Armenian Soviet Social-ist Republic. Bull World Health Organ, 53: 25–30.
29. Avagyan GA, Khachatryan EA, Sahakyan AE, et al (2012). Lyme Disease: A New Healthcare Issue In Armenia (in Arme-nian). Medicine Science and Education, 8:16–21.
30. Orkun Ö, Çakmak A, Nalbantoğlu S, Karaer Z (2020). Turkey tick news: A mo-lecular investigation into the presence of tick-borne pathogens in host-seeking ticks in Anatolia; Initial evidence of pu-tative vectors and pathogens, and foot-steps of a secretly rising vector tick, Haemaphysalis parva. Ticks Tick Borne Dis, 11 (3): 101373.
31. Szekeres S, Docters van Leeuwen A, et al (2019). Road-killed mammals provide insight into tick-borne bacterial patho-gen communities within urban habitats. Transbound Emerg Dis, 66 (1): 277-86.
32. Minichová L, Hamšíková Z, Mahríková L, et al (2017). Molecular evidence of Rick-ettsia spp. in ixodid ticks and rodents in suburban, natural and rural habitats in Slovakia. Parasit Vectors, 10 (1): 158.
33. Milutinović M, Masuzawa T, Tomanović S, et al (2008). Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Francisella tu-larensis and their co-infections in host-seeking Ixodes ricinus ticks collected in Serbia. Exp Appl Acarol, 45 (3-4): 171-83.
34. Kirkan, Ş., Erbaş, G., & Parin, U. (2017). Bacterial Tick-Borne Diseases of Live-stock Animals. In Livestock Science. IntechOpen, 116–124.
35. Perez G, Bastian S, Chastagner A, et al (2020). Relationships between landscape structure and the prevalence of two tick-borne infectious agents, Anaplasma phag-ocytophilum and Borrelia burgdorferi sensu lato, in small mammal communities. Landsc Ecol, 2: 435–51.
36. Halos L, Bord S, Cotté V, et al (2010). Eco-logical factors characterizing the preva-lence of bacterial tick-borne pathogens in Ixodes ricinus ticks in pastures and woodlands. Appl Environ Microbiol, 76 (13): 4413-20.
2. Michelet L, Delannoy S, Devillers E, et al (2014). High-throughput screening of tick-borne pathogens in Europe. Front Cell Infect Microbiol, 4: 103.
3. Cerar T, Strle F, Stupica D, et al (2016) Dif-ferences in genotype, clinical features, and inflammatory potential of Borrelia burgdorferi sensu stricto strains from Europe and the United States. Emerg Infect Dis, 22 (5): 818-27.
4. Murphy DS, Lee X, Larson SR, et al (2017) Prevalence and Distribution of Human and Tick Infections with the Ehrlichia muris-Like Agent and Anaplasma phago-cytophilum in Wisconsin, 2009-2015. Vector Borne Zoonotic Dis, 17 (4): 229-36.
5. Parola P, Raoult D (2001). Ticks and tick-borne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis, 32 (6): 897-928.
6. Cotté V, Bonnet S, Le Rhun D, et al (2008). Transmission of Bartonella henselae by Ix-odes ricinus. Emerg Infect Dis, 14 (7): 1074-80.
7. Fertner ME, Mølbak L, Boye Pihl TP, et al (2012). First detection of tick-borne "Candidatus Neoehrlichia mikurensis" in Denmark 2011. Euro Surveill, 17(8): 20096.
8. Dantas-Torres F, Chomel BB, Otranto D (2012). Ticks and tick-borne diseases: a One Health perspective. Trends Parasitol, 28 (10): 437-46.
9. Bouchard C, Beauchamp G, Nguon S, et al (2011). Associations between Ixodes scapu-laris ticks and small mammal hosts in a newly endemic zone in southeastern Canada: implications for Borrelia burgdor-feri transmission. Ticks Tick Borne Dis, 2 (4): 183-90.
10. Estrada-Peña A, Ayllón N, de la Fuente J (2012). Impact of climate trends on tick-borne pathogen transmission. Front Phys-iol, 3: 64.
11. James MC, Bowman AS, Forbes KJ, et al (2013). Environmental determinants of Ixodes ricinus ticks and the incidence of Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in Scotland. Parasitolo-gy, 140 (2): 237-46.
12. Githeko AK, Lindsay SW, Confalonieri UE, Patz JA (2000). Climate change and vec-tor-borne diseases: a regional analysis. Bull World Health Organ, 78 (9): 1136-47.
13. Illera JC, López G, García-Padilla L, Moreno Á (2017). Factors governing the prevalence and richness of avian haemosporidian communities within and between temperate mountains. PLoS One, 12 (9): e0184587.
14. Atoyan HA, Sargsyan M, Gevorgyan H, et al (2018). Determinants of avian malaria prevalence in mountainous Transcauca-sia. Biologia, 73: 1123–1130.
15. Vardanyan MV and Gevorgyan H (2009). The study of the epidemiological pecu-liarities of Piroplasmosis in the lowland zone of Armenia (in Armenia). In: In Annals: Actual Issues on the Epidemiology of Infection Diseases. Yerevan; 2009; 37–38.
16. Paronyan L, Zardaryan E, Bakunts V, et al (2016). A retrospective chart review study to describe selected zoonotic and arbo-viral etiologies in hospitalized febrile patients in the Republic of Armenia. BMC Infect Dis, 16 (1): 445.
17. Gevorgyan H, Grigoryan GG, Atoyan HA, et al (2019). Evidence of Crimean-Congo Haemorrhagic Fever Virus Occurrence in Ixodidae Ticks of Armenia. J Arthropod Borne Dis, 13 (1): 9-16.
18. Eremeeva M, Balayeva N, Roux V, et al (1995). Genomic and proteinic charac-terization of strain S, a rickettsia isolated from Rhipicephalus sanguineus ticks in Ar-menia. J Clin Microbiol, 33 (10): 2738-44.
19. Balayeva NM, Eremeeva ME, Raoult D (1994). Genomic identification of Rick-ettsia slovaca among spotted fever group rickettsia isolates from Dermacentor mar-ginatus in Armenia. Acta Virol, 38 (6): 321-5.
20. Moutailler S, Valiente Moro C, Vaumourin E, et al (2016). Co-infection of Ticks: The Rule Rather Than the Exception. PLoS Negl Trop Dis, 10 (3): e0004539.
21. Lejal E, Moutailler S, Šimo L, Vayssier-Taussat M, Pollet T (2019). Tick-borne pathogen detection in midgut and sali-vary glands of adult Ixodes ricinus. Parasit Vectors, 12 (1): 152.
22. Muradyan VS, Asmaryan ShG, and Sa-ghatelyan AK (2016). Assessment of space and time changes of NDVI (bio-mass) in Armenia’s mountain ecosys-tems using remote sensing data. Current Problems in Remote Sensing of the Earth from Space, 13: 49–60.
23. EarthExplorer. [cited 2018 Mar 12]. Availa-ble from: https://earthexplorer.usgs.gov/
24. Milich, L., & Weiss, E. (2000). GAC NDVI interannual coefficient of variation (CoV) images: Ground truth sampling of the Sahel along north-south transects. IJRS, 21 (2), 235–60.
25. AUA Acopian Center for the Environment GIS Data | Acopian Center for the En-vironment. [cited 2018 Mar 6]. Available from: http://ace.aua.am/gis-and-remote-sensing/vector-data/
26. Galuzo IG (1934). Some protozoan diseas-es of domestic animals in Armenia (in Russian). Zakavkazsk parasit Eksped v Armeniyu, 11: 29–47.
27. Airapetyan VG, Gazaryan VS, Grigoryan GA, and Mamikonyan MM (1960). Re-port on the work of the Armenian insti-tute of Animal Husbandry and Veteri-nary Science in the control of infectious and invasive diseases of farm animals (in Russian). Trudy Armyan Inst Zhivotnovod i Vet, 4: 211–31.
28. Tarasevit I V, Plotnikova LF, Jablonskaja VA, et al (1976). Natural foci of rick-ettsioses in the Armenian Soviet Social-ist Republic. Bull World Health Organ, 53: 25–30.
29. Avagyan GA, Khachatryan EA, Sahakyan AE, et al (2012). Lyme Disease: A New Healthcare Issue In Armenia (in Arme-nian). Medicine Science and Education, 8:16–21.
30. Orkun Ö, Çakmak A, Nalbantoğlu S, Karaer Z (2020). Turkey tick news: A mo-lecular investigation into the presence of tick-borne pathogens in host-seeking ticks in Anatolia; Initial evidence of pu-tative vectors and pathogens, and foot-steps of a secretly rising vector tick, Haemaphysalis parva. Ticks Tick Borne Dis, 11 (3): 101373.
31. Szekeres S, Docters van Leeuwen A, et al (2019). Road-killed mammals provide insight into tick-borne bacterial patho-gen communities within urban habitats. Transbound Emerg Dis, 66 (1): 277-86.
32. Minichová L, Hamšíková Z, Mahríková L, et al (2017). Molecular evidence of Rick-ettsia spp. in ixodid ticks and rodents in suburban, natural and rural habitats in Slovakia. Parasit Vectors, 10 (1): 158.
33. Milutinović M, Masuzawa T, Tomanović S, et al (2008). Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Francisella tu-larensis and their co-infections in host-seeking Ixodes ricinus ticks collected in Serbia. Exp Appl Acarol, 45 (3-4): 171-83.
34. Kirkan, Ş., Erbaş, G., & Parin, U. (2017). Bacterial Tick-Borne Diseases of Live-stock Animals. In Livestock Science. IntechOpen, 116–124.
35. Perez G, Bastian S, Chastagner A, et al (2020). Relationships between landscape structure and the prevalence of two tick-borne infectious agents, Anaplasma phag-ocytophilum and Borrelia burgdorferi sensu lato, in small mammal communities. Landsc Ecol, 2: 435–51.
36. Halos L, Bord S, Cotté V, et al (2010). Eco-logical factors characterizing the preva-lence of bacterial tick-borne pathogens in Ixodes ricinus ticks in pastures and woodlands. Appl Environ Microbiol, 76 (13): 4413-20.
| Files | ||
| Issue | Vol 53 No 11 (2024) | |
| Section | Original Article(s) | |
| Keywords | ||
| Tick-borne pathogen Bacterial pathogen Special variation Parasite ecology Armenia | ||
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How to Cite
1.
Aghayan S, Grigoryan G, Gevorgyan H, Harutyunyan T, Rukhkyan M, Muradyan V, Karadjian G, Marsot M, Moutailler S, Pollet T. Diversity and Distribution of Bacterial and Parasitic Tick-Borne Pathogens in Armenia, Transcaucasia. Iran J Public Health. 2024;53(11):2563-2571.
