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      Prevalence of Anaplasma phagocytophilum in Ixodes ricinus and Dermacentor reticulatus and Coinfection with Borrelia burgdorferi and Tick-Borne Encephalitis Virus in Western Ukraine

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          Abstract

          Introduction: Tick-borne encephalitis virus (TBEV) and Borrelia burgdorferi, the causative agent of Lyme disease (LD), are widespread in Western Ukraine. However, relatively little is known about Anaplasma phagocytophilum in this region. This study examined patterns of infection with A. phagocytophilum in two tick vectors compared with the better studied TBEV and B. burgdorferi.

          Materials: Ticks were collected in three different ecosystems of the Western Ukraine during 2009–2014. Samples were examined for pathogen detection using real-time polymerase chain reaction (PCR), and logistic regression models were developed to assess the significance of different factors.

          Results: Among the three selected ecological systems of the Western region of Ukraine, 5130 ticks belonging to Ixodes ricinus and Dermacentor reticulatus were collected between 2009 and 2014. They were grouped into 366 pools and were tested by PCR for A. phagocytophilum. A subsample (1620 ticks, 162 pools) of the ticks was concurrently tested by PCR for A. phagocytophilum, B. burgdorferi, and TBEV. Overall, there was no trend in the proportion of positive ticks across years ( p > 0.05). However, the prevalence of A. phagocytophilum was higher (27.4%) in I. ricinus than in D. reticulatus (15.9%) (OR = 2.69; 95% CI, 1.52–4.94 (Lower, Upper 95% CI)). Infection was more common in forested habitats (OR = 1.89; 95% CI, 1.07–3.36) and during the later summer–early autumn (3.78; 95% CI, 1.79–8.06). B. burgdorferi was found in 29.3% and 31.9% of I. ricinus and D. reticulatus, respectively; and TBEV was found in 6.3% and 14.5% of I. ricinus and D. reticulatus. Coinfection of A. phagocytophilum and B. burgdorferi occurred more often than chance and was more frequent than any other combination of pathogens ( p = 0.031).

          Conclusions: Our study is the first to explore the potential relationship between the ecosystems, vectors, and the presence of Human Granulocytic Anaplasmosis (HGA) and other tick-borne infections in Western Ukraine. Anaplasma demonstrated a greater prevalence in I. ricinus in the forested area in Western Ukraine. Altogether, HGA, LD, and tick-borne encephalitis (TBE) pathogens are actively circulating in these ecosystems and have the potential to coinfect vectors that might increase the risk of transmitting multiple pathogens to humans during host feeding by individual ticks.

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          Most cited references34

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          Coinfections acquired from ixodes ticks.

          The pathogens that cause Lyme disease (LD), human anaplasmosis, and babesiosis can coexist in Ixodes ticks and cause human coinfections. Although the risk of human coinfection differs by geographic location, the true prevalence of coinfecting pathogens among Ixodes ticks remains largely unknown for the majority of geographic locations. The prevalence of dually infected Ixodes ticks appears highest among ticks from regions of North America and Europe where LD is endemic, with reported prevalences of < or =28%. In North America and Europe, the majority of tick-borne coinfections occur among humans with diagnosed LD. Humans coinfected with LD and babesiosis appear to have more intense, prolonged symptoms than those with LD alone. Coinfected persons can also manifest diverse, influenza-like symptoms, and abnormal laboratory test results are frequently observed. Coinfecting pathogens might alter the efficiency of transmission, cause cooperative or competitive pathogen interactions, and alter disease severity among hosts. No prospective studies to assess the immunologic effects of coinfection among humans have been conducted, but animal models demonstrate that certain coinfections can modulate the immune response. Clinicians should consider the likelihood of coinfection when pursuing laboratory testing or selecting therapy for patients with tick-borne illness.
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            Climate change, biodiversity, ticks and tick-borne diseases: The butterfly effect

            We have killed wild animals for obtaining food and decimated forests for many reasons. Nowadays, we are burning fossil fuels as never before and even exploring petroleum in deep waters. The impact of these activities on our planet is now visible to the naked eye and the debate on climate change is warming up in scientific meetings and becoming a priority on the agenda of both scientists and policy decision makers. On the occasion of the Impact of Environmental Changes on Infectious Diseases (IECID) meeting, held in the 2015 in Sitges, Spain, I was invited to give a keynote talk on climate change, biodiversity, ticks and tick-borne diseases. The aim of the present article is to logically extend my rationale presented on the occasion of the IECID meeting. This article is not intended to be an exhaustive review, but an essay on climate change, biodiversity, ticks and tick-borne diseases. It may be anticipated that warmer winters and extended autumn and spring seasons will continue to drive the expansion of the distribution of some tick species (e.g., Ixodes ricinus) to northern latitudes and to higher altitudes. Nonetheless, further studies are advocated to improve our understanding of the complex interactions between landscape, climate, host communities (biodiversity), tick demography, pathogen diversity, human demography, human behaviour, economics, and politics, also considering all ecological processes (e.g., trophic cascades) and other possible interacting effects (e.g., mutual effects of increased greenhouse gas emissions and increased deforestation rates). The multitude of variables and interacting factors involved, and their complexity and dynamism, make tick-borne transmission systems beyond (current) human comprehension. That is, perhaps, the main reason for our inability to precisely predict new epidemics of vector-borne diseases in general.
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              Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in The Netherlands.

              From 2000 to 2004, ticks were collected by dragging a blanket in four habitat areas in The Netherlands: dunes, heather, forest, and a city park. Tick densities were calculated, and infection with Borrelia burgdorferi and Anaplasma and Ehrlichia species was investigated by reverse line blot analysis. The lowest tick density was observed in the heather area (1 to 8/100 m2). In the oak forest and city park, the tick densities ranged from 26 to 45/100 m2. The highest tick density was found in the dune area (139 to 551/100 m2). The infection rates varied significantly for the four study areas and years, ranging from 0.8 to 11. 5% for Borrelia spp. and 1 to 16% for Ehrlichia or Anaplasma (Ehrlichia/Anaplasma) spp. Borrelia infection rates were highest in the dunes, followed by the forest, the city park, and heather area. In contrast, Ehrlichia/Anaplasma was found most often in the forest and less often in the city park. The following Borrelia species were found: Borrelia sensu lato strains not identified to the species level (2.5%), B. afzelii (2.5%), B. valaisiana (0.9%), B. burgdorferi sensu stricto (0.13%), and B. garinii (0.13%). For Ehrlichia/Anaplasma species, Ehrlichia and Anaplasma spp. not identified to the species level (2.5%), Anaplasma schotti variant (3.5%), Anaplasma phagocytophilum variant (0.3%), and Ehrlichia canis (0.19%) were found. E. canis is reported for the first time in ticks in The Netherlands in this study. Borrelia lusitaniae, Ehrlichia chaffeensis, and the human granylocytic anaplasmosis agent were not detected. About 1.6% of the ticks were infected with both Borrelia and Ehrlichia/Anaplasma, which was higher than the frequency predicted from the individual infection rates, suggesting hosts with multiple infections or a possible selective advantage of coinfection.
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                Author and article information

                Journal
                Vector Borne Zoonotic Dis
                Vector Borne Zoonotic Dis
                vbz
                Vector Borne and Zoonotic Diseases
                Mary Ann Liebert, Inc., publishers (140 Huguenot Street, 3rd FloorNew Rochelle, NY 10801USA )
                1530-3667
                1557-7759
                01 November 2019
                25 October 2019
                25 October 2019
                : 19
                : 11
                : 793-801
                Affiliations
                [1]Research Institute of Epidemiology and Hygiene, Danylo Halytsky Lviv National Medical University, Lviv, Ukraine.
                Author notes
                [*]Address correspondence to: Iryna Ben, Research Institute of Epidemiology and Hygiene, Danylo Halytsky Lviv National Medical University, 12 Zelena Street, Lviv 79005, Ukraine iryna_ben@ 123456ukr.net
                Article
                10.1089/vbz.2019.2450
                10.1089/vbz.2019.2450
                6818487
                31211655
                8bfe963a-a47a-4339-92d3-2fc24f0a10ea
                © Iryna Ben and Ihor Lozynskyi 2019; Published by Mary Ann Liebert, Inc.

                This Open Access article is distributed under the terms of the Creative Commons Attribution Noncommercial License ( http://creativecommons.org/licenses/by-nc/4.0/) which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and the source are cited.

                History
                Page count
                Figures: 3, Tables: 3, References: 39, Pages: 9
                Categories
                Original Articles

                human granulocytic anaplasmosis,anaplasma phagocytophilum,borrelia burgdorferi,tick-borne encephalitis virus,tick-borne infections,ticks,ukraine

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