Detection Of Selected Pathogens In Ixodid Ticks Collected From Animals And Vegetation In Five Regions Of Ukraine

Background Over the last few decades tick-borne diseases have emerged as an increasingly significant public health problem. The distribution and prevalence of zoonotic pathogens infecting ixodid ticks from Western Europe have been extensively examined. However, data on ticks and tick-borne pathogens in Eastern Europe, particularly Ukraine are scarce. The objective of the current study was, therefore, to investigate the prevalence rates of Anaplasma phagocytophilum , the Anaplasmataceae family, Rickettsia spp., Babesia spp., Bartonella spp., and Borrelia burgdorferi sensu lato in engorged and questing ixodid ticks collected from five administrative oblasts (regions) of Ukraine, namely Chernivtsi, Khmelnytskyi, Kyiv, Ternopil, and Vinnytsia.Methods The ticks were collected from both wild and domestic animals and from vegetation. Of 524 ixodid ticks collected, 3, 99, and 422 ticks were identified as Ixodes hexagonus , Ixodes ricinus, and Dermacentor reticulatus , respectively. DNA samples individually extracted from 168 questing and 354 engorged adult ticks were subjected to pathogen-specific PCR analyses.Results The mean prevalence rates in all I. ricinus and D. reticulatus ticks were, respectively: 10.3% (10/97) and 2.8% (12/422) for A. phagocytophilum ; 69.1% (67/97) and 52.1% (220/422) for the Anaplasmataceae family; 24.7% (24/97) and 27.7% (117/422) for Rickettsia spp.; 3.1% (3/97) and 1.4% (6/422) for Babesia spp.; and 9.3% (9/97) and 4.7% (20/422) for Bartonella spp. Overall, between the five cities, there was no significant difference in the prevalence rates of any of the pathogens for the respective ticks ( p >0.05). The prevalence of B. burgdorferi s.l. in the engorged and questing I. ricinus ticks varied from 26.7% and 0% to 44.4% and 14.3%, respectively, with no statistical significance identified between the five cities ( p >0.05).Conclusions In addition to reporting the updated data for Kyiv and Ternopil, this study is the first to provide the prevalence rates of the tick-borne pathogens for Chernivtsi, Khmelnytskyi, and Vinnytsia. This investigation is also the first to detect Ca. N. mikurensis in ixodid ticks from Ukraine. These new data will be useful for medical and veterinary practitioners as well as public health officials when diagnosing infections and when implementing measures to combat tick-borne diseases in Ukraine.

[1]  D. Threadgill,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. , 2019, Vector borne and zoonotic diseases.

[2]  J. Coburn,et al.  Recent discoveries and advancements in research on the Lyme disease spirochete Borrelia burgdorferi , 2019, F1000Research.

[3]  M. Embers,et al.  Human Bartonellosis: An Underappreciated Public Health Problem? , 2019, Tropical medicine and infectious disease.

[4]  G. von Samson-Himmelstjerna,et al.  Dermacentor reticulatus in Berlin/Brandenburg (Germany): Activity patterns and associated pathogens. , 2019, Ticks and tick-borne diseases.

[5]  Anne E Jones,et al.  Impact of recent and future climate change on vector‐borne diseases , 2018, Annals of the New York Academy of Sciences.

[6]  H. Zeller,et al.  An updated meta-analysis of the distribution and prevalence of Borrelia burgdorferi s.l. in ticks in Europe , 2018, International Journal of Health Geographics.

[7]  N. Tikunova,et al.  Dog survey in Russian veterinary hospitals: tick identification and molecular detection of tick-borne pathogens , 2018, Parasites & Vectors.

[8]  V. Ridde,et al.  Scoping review on vector-borne diseases in urban areas: transmission dynamics, vectorial capacity and co-infection , 2018, Infectious Diseases of Poverty.

[9]  P. Sobczak,et al.  Prevalence of Borrelia Burgdorferi Sensu Lato in Ticks from the Ternopil Region in Ukraine , 2018, Journal of veterinary research.

[10]  P. Fournier,et al.  A Concise Review of the Epidemiology and Diagnostics of Rickettsioses: Rickettsia and Orientia spp , 2018, Journal of Clinical Microbiology.

[11]  C. Beard,et al.  Vital Signs: Trends in Reported Vectorborne Disease Cases — United States and Territories, 2004–2016 , 2018, MMWR. Morbidity and mortality weekly report.

[12]  G. Moore,et al.  ACVIM consensus update on Lyme borreliosis in dogs and cats , 2018, Journal of veterinary internal medicine.

[13]  R. Wall,et al.  Anaplasma phagocytophilum, Bartonella spp., haemoplasma species and Hepatozoon spp. in ticks infesting cats: a large-scale survey , 2018, Parasites & Vectors.

[14]  J. Oteo,et al.  ‘Candidatus Neoehrlichia mikurensis’ in Europe , 2018, New microbes and new infections.

[15]  D. C. Gillis,et al.  Diversity of Borrelia spirochetes and other zoonotic agents in ticks from Kyiv, Ukraine. , 2017, Ticks and tick-borne diseases.

[16]  A. Sopińska,et al.  Comparison of the occurrence of tick-borne diseases in ticks collected from vegetation and animals in the same area , 2018 .

[17]  C. Strube,et al.  A 10-year surveillance of Rickettsiales (Rickettsia spp. and Anaplasma phagocytophilum) in the city of Hanover, Germany, reveals Rickettsia spp. as emerging pathogens in ticks , 2017, Parasites & Vectors.

[18]  M. Korda,et al.  EPIDEMIOLOGICAL SITUATION OF LYME BORRELIOSIS AND DIAGNOSIS STANDARDS IN POLAND AND UKRAINE , 2017 .

[19]  M. Malý,et al.  Detection of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in questing ticks Ixodes ricinus from the Czech Republic. , 2017, Ticks and tick-borne diseases.

[20]  C. C. van den Wijngaard,et al.  The cost of Lyme borreliosis , 2017, European journal of public health.

[21]  E. Thiry,et al.  Anaplasma, Ehrlichia and Rickettsia species infections in cats: European guidelines from the ABCD on prevention and management , 2017, Journal of feline medicine and surgery.

[22]  J. Waldenström,et al.  Canine tick-borne diseases in pet dogs from Romania , 2017, Parasites & Vectors.

[23]  B. Peťko,et al.  Emergence of tick-borne pathogens (Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Ricketsia raoultii and Babesia microti) in the Kyiv urban parks, Ukraine. , 2017, Ticks and tick-borne diseases.

[24]  R. Sykes,et al.  An estimate of Lyme borreliosis incidence in Western Europe† , 2016, Journal of public health.

[25]  G. Scoles,et al.  Ixodid ticks in the megapolis of Kyiv, Ukraine. , 2017, Ticks and tick-borne diseases.

[26]  S. Tylewska-wierzbanowska,et al.  Rickettsia raoultii in Dermacentor reticulatus Ticks, Chernobyl Exclusion Zone, Ukraine, 2010 , 2016, Emerging infectious diseases.

[27]  G. Stanek,et al.  Detection of Bartonella spp. in Ixodes ricinus ticks and Bartonella seroprevalence in human populations. , 2016, Ticks and tick-borne diseases.

[28]  A. Estrada-Peña,et al.  A review of canine babesiosis: the European perspective , 2016, Parasites & Vectors.

[29]  M. Stanko,et al.  Presence of Candidatus Neoehrlichia mikurensis and Babesia microti in rodents and two tick species (Ixodes ricinus and Ixodes trianguliceps) in Slovakia. , 2016, Ticks and tick-borne diseases.

[30]  A. Pawełczyk,et al.  Pathogens vectored by the tick, Dermacentor reticulatus, in endemic regions and zones of expansion in Poland , 2015, Parasites & Vectors.

[31]  J. Dutkiewicz,et al.  Bartonella henselae in Eastern Poland: The Relationship between Tick Infection Rates and the Serological Response of Individuals Occupationally Exposed to Tick Bites , 2015, Journal of vector ecology : journal of the Society for Vector Ecology.

[32]  B. Peťko,et al.  The infection of questing Dermacentor reticulatus ticks with Babesia canis and Anaplasma phagocytophilum in the Chernobyl exclusion zone. , 2014, Veterinary parasitology.

[33]  R. Václav,et al.  Candidatus Neoehrlichia mikurensis and its co-circulation with Anaplasma phagocytophilum in Ixodes ricinus ticks across ecologically different habitats of Central Europe , 2014, Parasites & Vectors.

[34]  V. Majláthová,et al.  Anaplasma infections in ticks and reservoir host from Slovakia. , 2014, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[35]  D. Kiewra,et al.  The prevalence of Anaplasma phagocytophilum in questing Ixodes ricinus ticks in SW Poland. , 2014, Polish journal of microbiology.

[36]  B. Kuehn CDC estimates 300,000 US cases of Lyme disease annually. , 2013, JAMA.

[37]  B. Peťko,et al.  Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia , 2013, Parasites & Vectors.

[38]  E. G. Granquist,et al.  Anaplasma phagocytophilum—a widespread multi-host pathogen with highly adaptive strategies , 2013, Front. Cell. Infect. Microbiol..

[39]  H. Sprong,et al.  Spotted fever group rickettsiae in Dermacentor reticulatus and Haemaphysalis punctata ticks in the UK , 2013, Parasites & Vectors.

[40]  G. von Samson-Himmelstjerna,et al.  A Novel High-Resolution Melt PCR Assay Discriminates Anaplasma phagocytophilum and “Candidatus Neoehrlichia mikurensis” , 2013, Journal of Clinical Microbiology.

[41]  J. Fuente,et al.  Prevalence of tick-borne pathogens in adult Dermacentor spp. ticks from nine collection sites in France. , 2013, Vector borne and zoonotic diseases.

[42]  G. Ignatyev,et al.  Prevalence of Tick-Borne Pathogens in Ixodes ricinus and Dermacentor reticulatus Ticks from Different Geographical Locations in Belarus , 2013, PloS one.

[43]  M. Madder,et al.  Tick-borne infections (including zoonoses) in Europe and the Mediterranean Basin , 2012 .

[44]  D. Morrison,et al.  Babesia: a world emerging. , 2012, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[45]  E. Špitalská,et al.  Rickettsia slovaca and Rickettsia raoultii in Dermacentor marginatus and Dermacentor reticulatus ticks from Slovak Republic , 2012, Experimental and Applied Acarology.

[46]  Maureen H Diaz,et al.  Development of a Novel Genus-Specific Real-Time PCR Assay for Detection and Differentiation of Bartonella Species and Genotypes , 2012, Journal of Clinical Microbiology.

[47]  A. Shulgan,et al.  Natural Focal Transmissible Infections with Neurological Manifestations in Ukraine , 2011 .

[48]  M. Bednář,et al.  West-to-east differences of Babesia canis canis prevalence in Dermacentor reticulatus ticks in Slovakia. , 2011, Veterinary parasitology.

[49]  M. Neteler,et al.  Lyme borreliosis in Europe. , 2011, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[50]  E. Breitschwerdt,et al.  “Candidatus Neoehrlichia mikurensis” Infection in a Dog from Germany , 2011, Journal of Clinical Microbiology.

[51]  R. Weber,et al.  Septicemia Caused by Tick-borne Bacterial Pathogen Candidatus Neoehrlichia mikurensis , 2010, Emerging infectious diseases.

[52]  C. Bogdan,et al.  Detection of “Candidatus Neoehrlichia mikurensis” in Two Patients with Severe Febrile Illnesses: Evidence for a European Sequence Variant , 2010, Journal of Clinical Microbiology.

[53]  C. Wennerås,et al.  First Case of Human “Candidatus Neoehrlichia mikurensis” Infection in a Febrile Patient with Chronic Lymphocytic Leukemia , 2010, Journal of Clinical Microbiology.

[54]  R. Vonthein,et al.  Prevalence of Bartonella henselae and Borrelia burgdorferi Sensu Lato DNA in Ixodes ricinus Ticks in Europe , 2010, Applied and Environmental Microbiology.

[55]  D. Raoult,et al.  Detection of spotted fever group rickettsiae and family Anaplasmataceae in Ixodes ricinus ticks from Republic of Moldova and Eastern Ukraine. , 2009, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[56]  E. Breitschwerdt,et al.  PCR detection of Bartonella bovis and Bartonella henselae in the blood of beef cattle. , 2009, Veterinary microbiology.

[57]  E. Podsiadły,et al.  Rickettsia spp. in Ticks, Poland , 2009, Emerging infectious diseases.

[58]  A. Paulauskas,et al.  Prevalence of Anaplasma phagocytophilum and Babesia divergens in Ixodes ricinus ticks from Lithuania and Norway , 2008 .

[59]  E. Breitschwerdt,et al.  Vector transmission of Bartonella species with emphasis on the potential for tick transmission , 2008, Medical and veterinary entomology.

[60]  Armand Sánchez,et al.  Vector-borne infections in cats: molecular study in Barcelona area (Spain). , 2008, Veterinary parasitology.

[61]  P. Branny,et al.  Molecular evidence ofBartonella DNA in ixodid ticks in Czechia , 2008, Folia Microbiologica.

[62]  A. Movila,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 , 2007, Experimental and Applied Acarology.

[63]  A. Nijhof,et al.  Ticks and associated pathogens collected from domestic animals in the Netherlands. , 2007, Vector borne and zoonotic diseases.

[64]  J. Stańczak Detection of spotted fever group (SFG) rickettsiae in Dermacentor reticulatus (Acari: Ixodidae) in Poland. , 2006, International journal of medical microbiology : IJMM.

[65]  M. Vayssier-Taussat,et al.  Effects of Cow Age and Pregnancy on Bartonella Infection in a Herd of Dairy Cattle , 2006, Journal of Clinical Microbiology.

[66]  T. Hartung,et al.  Prevalence of Borrelia burgdorferi Sensu Lato Genospecies in Ixodes ricinus Ticks in Europe: a Metaanalysis , 2005, Applied and Environmental Microbiology.

[67]  S Harrus,et al.  Drivers for the emergence and re-emergence of vector-borne protozoal and bacterial diseases. , 2005, International journal for parasitology.

[68]  O. Morozova,et al.  [Detection of the Bartonella DNA by the method of nested PCR in patients after tick bites in Novosibirsk region]. , 2005, Molekuliarnaia genetika, mikrobiologiia i virusologiia.

[69]  E. Isogai,et al.  Ultrastructure and phylogenetic analysis of 'Candidatus Neoehrlichia mikurensis' in the family Anaplasmataceae, isolated from wild rats and found in Ixodes ovatus ticks. , 2004, International journal of systematic and evolutionary microbiology.

[70]  M. Levin,et al.  Acquisition of different isolates of Anaplasma phagocytophilum by Ixodes scapularis from a model animal. , 2004, Vector borne and zoonotic diseases.

[71]  P. Radziwon,et al.  Zakazenia zubrow z Puszczy Bialowieskiej bakteriami Anaplasma phagocytophilum , 2004 .

[72]  E. Breitschwerdt,et al.  Development and Evaluation of a Seminested PCR for Detection and Differentiation of Babesia gibsoni (Asian Genotype) and B. canis DNA in Canine Blood Samples , 2003, Journal of Clinical Microbiology.

[73]  S. Ray,et al.  Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and , 2001, International journal of systematic and evolutionary microbiology.

[74]  D. Raoult,et al.  Phylogeny of Rickettsia spp. inferred by comparing sequences of 'gene D', which encodes an intracytoplasmic protein. , 2001, International journal of systematic and evolutionary microbiology.

[75]  A. Trees On ticks and tick-borne diseases. , 1999, Parasitology today.

[76]  L. Schouls,et al.  Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks. , 1999, Journal of clinical microbiology.

[77]  J. L. Montagne,et al.  Emerging infectious diseases. , 1994, The Journal of infectious diseases.

[78]  R. Marconi,et al.  C F Garon nucleotide analysis . disease isolates by 16 S rRNA signature for species-specific identification of Lyme primer sets for diagnosis of Lyme disease and Development of polymerase chain reaction , 1992 .