Restricted accessResearch articleFirst published online 2019-07
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
The 26th of April 2016 marked 30 years since the Chernobyl accident has occurred in Ukraine. As a result, the uninhabited Chernobyl region has been directly exposed to ionizing radiation for >30 years. Most work has focused on identifying associations between levels of radiation and the abundance, distribution, and mutation rates of plants and animals. Much less, however, is known about microbial communities in this affected region. To date, there are no reports on the prevalence of any tick-borne pathogens in Ixodes ricinus ticks from the Chernobyl exclusion zone (CEZ). The objective of our study was to examine the abundance of I. ricinus and Dermacentor reticulatus ticks in the CEZ and to investigate the prevalence of Borrelia burgdorferi sensu lato (s.l.) and other zoonotic agents in these ixodid ticks.
Methods:
A total of 260 questing I. ricinus and 100 D. reticulatus adult ticks were individually polymerase chain reaction analyzed for the presence of Anaplasma phagocytophilum, Babesia spp., Bartonella spp., Borrelia burgdorferi s.l., Francisella tularensis, and/or Rickettsia spp.
Results:
The respective infections rates were identified and compared with those of ixodid ticks that were concurrently collected from Kyiv. The significant differences between the infection rates of the CEZ and Kyiv ticks were observed for Rickettsia raoultii in D. reticulatus ticks (53.0% vs. 35.7%, respectively; p < 0.05) and Bartonella spp. (8.1% vs. 2.7%; P < 0.05) in I. ricinus ticks.
Conclusions:
Although the current data clearly demonstrated that the prevalence of some zoonotic pathogens were significantly higher in the ixodid ticks from the CEZ, a more comprehensive systematic approach is required to examine the causal effect of long-term ionizing radiation on adaptive changes of tick-borne pathogens.
Get full access to this article
View all access options for this article.
References
1.
AkimovIA, NebogatkinIV. Diversity of ixodid ticks (Acari: Ixodidae) in megapolis Kyiv. Fundamental and applied aspects of the study of parasitic arthropods in the 21st century. St. Petersburg, Russia, 2013.
2.
AlbertiA, ZobbaR, ChessaB, AddisMF, et al.Equine and canine Anaplasma phagocytophilum strains isolated on the island of Sardinia (Italy) are phylogenetically related to pathogenic strains from the United States. Applied Environmental Microbiology, 2005; 71:6418–6422.
3.
AngelakisE, BilleterSA, BreitschwerdtEB, ChomelBB, et al.Potential for tick-borne bartonelloses. Emerging Infectious Diseases, 2010; 16:385–391.
4.
BakkenJS, DumlerJS. Human granulocytic anaplasmosis. Infect Dis Clin North Am, 2015; 29:341–355.
5.
BarnsSM, GrowCC, OkinakaRT, KeimP, et al.Detection of diverse new Francisella-like bacteria in environmental samples. Appl Environ Microbiol, 2005; 71:5494–5500.
6.
BiletskaH, LozynskiyI, DrulO, SemenyshynO, et al.Natural focal transmissible infections with neurological manifestations in Ukraine. In: RůžekD, ed. Flavivirus encephalitis: InTech, Chapters published; 2011:490.
7.
BiletskaH, PodavalenkoL, SemenyshynO, LozynskyjI, et al.Study of Lyme borreliosis in Ukraine. International Journal of Medical Microbiology, 2008; 298:154–160.
8.
Brites-NetoJ, DuarteKM, MartinsTF. Tick-borne infections in human and animal population worldwide. Vet World, 2015; 8:301–315.
9.
BunikisJ, GarpmoU, TsaoJ, BerglundJ, et al.Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology, 2004; 150:1741–1755.
10.
CamachoC, CoulourisG, AvagyanV, MaN, et al.BLAST+: Architecture and applications. BMC Bioinformatics, 2009; 10:421.
11.
CampbellI.Chi-squared and Fisher-Irwin tests of two-by-two tables with small sample recommendations. Stat Med, 2007; 26:3661–3675.
12.
CasatiS, SagerH, GernL, PiffarettiJC. Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med, 2006; 13:65–70.
13.
ColwellDD, Dantas-TorresF, OtrantoD. Vector-borne parasitic zoonoses: Emerging scenarios and new perspectives. Vet Parasitol, 2011; 182:14–21.
14.
DayMJ.One health: The importance of companion animal vector-borne diseases. Parasites & Vectors, 2011; 4:49.
15.
DidykYM, BlaňarováL, PogrebnyakS, AkimovI, et al.Emergence of tick-borne pathogens (Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Rickettsia raoultii and Babesia microti) in the Kyiv urban parks, Ukraine. Ticks Tick Borne Dis. 2017.
16.
FilippovaN.Ticks of subfamily Amblyominae//Arachnids. Nauka; 1997:446.
GyuraneczM, RigoK, DanA, FoldvariG, et al.Investigation of the ecology of Francisella tularensis during an inter-epizootic period. Vector Borne Zoonotic Dis, 2011; 11:1031–1035.
19.
HerrmannC, GernL, VoordouwMJ. Species co-occurrence patterns among Lyme borreliosis pathogens in the tick vector Ixodes ricinus. Appl Environ Microbiol, 2013; 79:7273–7280.
20.
HinckleyAF, ConnallyNP, MeekJI, JohnsonBJ, et al.Lyme disease testing by large commercial laboratories in the United States. Clin Infect Dis, 2014; 59:676–681.
HunfeldKP, HildebrandtA, GrayJS. Babesiosis: Recent insights into an ancient disease. Int J Parasitol, 2008; 38:1219–1237.
23.
JinH, WeiF, LiuQ, QianJ. Epidemiology and control of human granulocytic anaplasmosis: A systematic review. Vector Borne Zoonotic Dis, 2012; 12:269–274.
KarbowiakG, VíchováB, SlivinskaK, WerszkoJ, et al.The infection of questing Dermacentor reticulatus ticks with Babesia canis and Anaplasma phagocytophilum in the Chernobyl exclusion zone. Vet Parasitol, 2014; 204:372–375.
26.
KurtenbachK, De MichelisS, SewellHS, EttiS, et al.Distinct combinations of Borrelia burgdorferi sensu lato genospecies found in individual questing ticks from Europe. Appl Environ Microbiol, 2001; 67:4926–4929.
27.
LindgrenE, JaensonTGT. Lyme borreliosis in Europe: Influences of climate and climate change, epidemiology and adaptation measures. In: MenneB, EbiKL, eds. Climate change and adaptation strategies for human health. Darmstadt, Germany: Steinkopff; 2006:157–188.
28.
MaksimovaS.The effect of radioactive contamination caused by the Chernobyl nuclear accident on Diplopoda communities. Acta Zoologica Lituanica, 2002; 12:90–94.
29.
MaxamAM, GilbertW. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol, 1980; 65:499–560.
30.
MietelskiJW, MaksimovaS, SzwalkoP, WnukK, et al.Plutonium, 137Cs and 90Sr in selected invertebrates from some areas around Chernobyl nuclear power plant. J Environ Radioact, 2010; 101:488–493.
31.
MollerAP, Bonisoli-AlquatiA, MousseauTA, RudolfsenG. Aspermy, sperm quality and radiation in Chernobyl birds. PLoS One, 2014; 9:e100296.
32.
MollerAP, MousseauTA. Biological consequences of Chernobyl: 20 years on. Trends Ecol Evol, 2006; 21:200–207.
33.
MousseauTA, MollerAP. Genetic and ecological studies of animals in Chernobyl and Fukushima. J Hered, 2014; 105:704–709.
34.
MovilaA, DeriabinaT, MorozovA, SitnicovaN, et al.Abundance of adult ticks (Acari: Ixodidae) in the Chernobyl nuclear power plant exclusion zone. J Parasitol, 2012; 98:883–884.
35.
MovilaA, MorozovA, SitnicovaN. Genetic polymorphism of 12S rRNA gene among Dermacentor reticulatus Fabricius ticks in the Chernobyl Nuclear Power Plant Exclusion Zone. J Parasitol, 2013; 99:40–43.
36.
NebogatkinIV, ShulganAM, NovohatniyYO, VydaykoNB, et al.Epidemiology of Lyme borreliosis and ixodid ticks in Ukraine, 2016 Important infectious diseases. Current aspects of clinical diagnostics, treatment, and prophylaxis. Kyiv, Ukraine. 2017:43–44.
37.
NelsonCA, MooreAR, PereaAE, MeadPS. Cat scratch disease: U.S. Clinicians' experience and knowledge. Zoonoses Public Health, 2017.
38.
OskolkovBY, BondarkovMD, GaschakSP, MaksimenkoAM, et al.Radiation dose assessment for the biota of terrestrial ecosystems in the shoreline zone of the Chernobyl nuclear power plant cooling pond. Health Phys, 2011; 101:349–361.
39.
ParolaP, PaddockCD, SocolovschiC, LabrunaMB, et al.Update on tick-borne rickettsioses around the world: A geographic approach. Clin Microbiol Rev, 2013; 26:657–702.
40.
PetterssonJH, ShiM, BohlinJ, EldholmV, et al.Characterizing the virome of Ixodes ricinus ticks from northern Europe. Sci Rep, 2017; 7:10870.
41.
PhanJN, LuCR, BenderWG, SmoakRM3rd, et al.Molecular detection and identification of Rickettsia species in Ixodes pacificus in California. Vector Borne Zoonotic Dis, 2011; 11:957–961.
42.
RarVA, FomenkoNV, DobrotvorskyAK, LivanovaNN, et al.Tickborne pathogen detection, Western Siberia, Russia. Emerg Infect Dis, 2005; 11:1708–1715.
43.
RauterC, HartungT. Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: A metaanalysis. Appl Environ Microbiol, 2005; 71:7203–7216.
44.
ReyeAL, StegniyV, MishaevaNP, VelhinS, 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.
45.
RichardsonJTE.The analysis of 2 × 2 contingency tables-Yet again. Statistics in Medicine, 2011; 30:890–890.
46.
RizzoliA, HauffeHC, CarpiG, Vourc'hGI, et al.Lyme borreliosis in Europe. Eurosurveillance, 2011; 16:2–9.
47.
RogovskyyA, BatoolM, GillisDC, HolmanPJ, et al.Diversity of Borrelia spirochetes and other zoonotic agents in ticks from Kyiv, Ukraine. Ticks Tick Borne Dis, 2018; 9:404–409.
48.
RogovskyyAS, NebogatkinIV, ScolesGA. Ixodid ticks in the megapolis of Kyiv, Ukraine. Ticks Tick Borne Dis, 2017; 8:99–102.
49.
RouxV, RydkinaE, EremeevaM, RaoultD. Citrate synthase gene comparison, a new tool for phylogenetic analysis, and its application for the rickettsiae. Int J Syst Bacteriol, 1997; 47:252–261.
50.
RubelF, BruggerK, MonazahianM, HabedankB, et al.The first German map of georeferenced ixodid tick locations. Parasit Vectors, 2014; 7:477.
51.
RubelF, BruggerK, PfefferM, Chitimia-DoblerL, et al.Geographical distribution of Dermacentor marginatus and Dermacentor reticulatus in Europe. Ticks Tick Borne Dis, 2016; 7:224–233.
StanekG, FingerleV, HunfeldKP, JaulhacB, et al.Lyme borreliosis: Clinical case definitions for diagnosis and management in Europe. Clinical Microbiology and Infection, 2011; 17:69–79.
54.
StaplesJE, KubotaKA, ChalcraftLG, MeadPS, et al.Epidemiologic and molecular analysis of human tularemia, United States, 1964–2004. Emerg Infect Dis, 2006; 12:1113–1118.
55.
TomassoneL, PortilloA, NovakovaM, de SousaR, et al.Neglected aspects of tick-borne rickettsioses. Parasit Vectors, 2018; 11:263.
56.
van den WijngaardCC, HofhuisA, SimoesM, RoodE, et al.Surveillance perspective on Lyme borreliosis across the European Union and European Economic Area. Euro Surveill, 2017; 22.
57.
VannierE, KrausePJ. Human babesiosis. N Engl J Med, 2012; 366:2397–2407.
58.
VershininE, VershininP. A tick quantification method. Current questions of biology in the Baikal region. Irkutsk, Russia. 2009:54–55 (In Russian).
59.
WoodH, ArtsobH. Spotted fever group rickettsiae: A brief review and a Canadian perspective. Zoonoses Public Health, 2012; 59Suppl 2:65–79.
60.
YablokovAV, NesterenkoVB, NesterenkoAV. Chapter III. Consequences of the Chernobyl catastrophe for the environment. Ann N Y Acad Sci, 2009; 1181:221–222.
61.
YablokovAV. 9. Chernobyl's radioactive impact on flora. Ann N Y Acad Sci, 2009; 1181:237–254.
62.
ZeaiterZ, FournierPE, RaoultD. Genomic variation of Bartonella henselae strains detected in lymph nodes of patients with cat scratch disease. J Clin Microbiol, 2002; 40:1023–1030.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
