{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T03:45:51Z","timestamp":1790480751495,"version":"4.1.0"},"reference-count":39,"publisher":"SAGE Publications","issue":"11","license":[{"start":{"date-parts":[[2019,10,25]],"date-time":"2019-10-25T00:00:00Z","timestamp":1571961600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"},{"start":{"date-parts":[[2019,10,25]],"date-time":"2019-10-25T00:00:00Z","timestamp":1571961600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.sagepub.com\/page\/policies\/text-and-data-mining-license"}],"content-domain":{"domain":["journals.sagepub.com"],"crossmark-restriction":true},"short-container-title":["Vector-Borne and Zoonotic Diseases"],"published-print":{"date-parts":[[2019,11]]},"abstract":"<jats:sec>\n                    <jats:title>Introduction:<\/jats:title>\n                    <jats:p>\n                      Tick-borne encephalitis virus (TBEV) and\n                      <jats:italic toggle=\"yes\">Borrelia burgdorferi<\/jats:italic>\n                      , the causative agent of Lyme disease (LD), are widespread in Western Ukraine. However, relatively little is known about\n                      <jats:italic toggle=\"yes\">Anaplasma phagocytophilum<\/jats:italic>\n                      in this region. This study examined patterns of infection with\n                      <jats:italic toggle=\"yes\">A. phagocytophilum<\/jats:italic>\n                      in two tick vectors compared with the better studied TBEV and\n                      <jats:italic toggle=\"yes\">B. burgdorferi.<\/jats:italic>\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Materials:<\/jats:title>\n                    <jats:p>Ticks were collected in three different ecosystems of the Western Ukraine during 2009\u20132014. 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.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results:<\/jats:title>\n                    <jats:p>\n                      Among the three selected ecological systems of the Western region of Ukraine, 5130 ticks belonging to\n                      <jats:italic toggle=\"yes\">Ixodes ricinus<\/jats:italic>\n                      and\n                      <jats:italic toggle=\"yes\">Dermacentor reticulatus<\/jats:italic>\n                      were collected between 2009 and 2014. They were grouped into 366 pools and were tested by PCR for\n                      <jats:italic toggle=\"yes\">A. phagocytophilum<\/jats:italic>\n                      . A subsample (1620 ticks, 162 pools) of the ticks was concurrently tested by PCR for\n                      <jats:italic toggle=\"yes\">A. phagocytophilum<\/jats:italic>\n                      ,\n                      <jats:italic toggle=\"yes\">B. burgdorferi<\/jats:italic>\n                      , and TBEV. Overall, there was no trend in the proportion of positive ticks across years (\n                      <jats:italic toggle=\"yes\">p<\/jats:italic>\n                      \u2009&gt;\u20090.05). However, the prevalence of\n                      <jats:italic toggle=\"yes\">A. phagocytophilum<\/jats:italic>\n                      was higher (27.4%) in\n                      <jats:italic toggle=\"yes\">I. ricinus<\/jats:italic>\n                      than in\n                      <jats:italic toggle=\"yes\">D. reticulatus<\/jats:italic>\n                      (15.9%) (OR\u2009=\u20092.69; 95% CI, 1.52\u20134.94 (Lower, Upper 95% CI)). Infection was more common in forested habitats (OR\u2009=\u20091.89; 95% CI, 1.07\u20133.36) and during the later summer\u2013early autumn (3.78; 95% CI, 1.79\u20138.06).\n                      <jats:italic toggle=\"yes\">B. burgdorferi<\/jats:italic>\n                      was found in 29.3% and 31.9% of\n                      <jats:italic toggle=\"yes\">I. ricinus<\/jats:italic>\n                      and\n                      <jats:italic toggle=\"yes\">D. reticulatus<\/jats:italic>\n                      , respectively; and TBEV was found in 6.3% and 14.5% of\n                      <jats:italic toggle=\"yes\">I. ricinus<\/jats:italic>\n                      and\n                      <jats:italic toggle=\"yes\">D. reticulatus<\/jats:italic>\n                      . Coinfection of\n                      <jats:italic toggle=\"yes\">A. phagocytophilum<\/jats:italic>\n                      and\n                      <jats:italic toggle=\"yes\">B. burgdorferi<\/jats:italic>\n                      occurred more often than chance and was more frequent than any other combination of pathogens (\n                      <jats:italic toggle=\"yes\">p<\/jats:italic>\n                      \u2009=\u20090.031).\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions:<\/jats:title>\n                    <jats:p>\n                      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.\n                      <jats:italic toggle=\"yes\">Anaplasma<\/jats:italic>\n                      demonstrated a greater prevalence in\n                      <jats:italic toggle=\"yes\">I. ricinus<\/jats:italic>\n                      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.\n                    <\/jats:p>\n                  <\/jats:sec>","DOI":"10.1089\/vbz.2019.2450","type":"journal-article","created":{"date-parts":[[2019,6,18]],"date-time":"2019-06-18T14:05:40Z","timestamp":1560866740000},"page":"793-801","update-policy":"https:\/\/doi.org\/10.1177\/sage-journals-update-policy","source":"Crossref","is-referenced-by-count":31,"title":["Prevalence of\n                    <i>Anaplasma phagocytophilum<\/i>\n                    in\n                    <i>Ixodes ricinus<\/i>\n                    and\n                    <i>Dermacentor reticulatus<\/i>\n                    and Coinfection with\n                    <i>Borrelia burgdorferi<\/i>\n                    and Tick-Borne Encephalitis Virus in Western Ukraine"],"prefix":"10.1177","volume":"19","author":[{"given":"Iryna","family":"Ben","sequence":"first","affiliation":[{"name":"Research Institute of Epidemiology and Hygiene, Danylo Halytsky Lviv National Medical University, Lviv, Ukraine."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ihor","family":"Lozynskyi","sequence":"additional","affiliation":[{"name":"Research Institute of Epidemiology and Hygiene, Danylo Halytsky Lviv National Medical University, Lviv, Ukraine."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"179","published-online":{"date-parts":[[2019,10,25]]},"reference":[{"key":"e_1_3_3_2_1","doi-asserted-by":"publisher","DOI":"10.1089\/vbz.2012.0987"},{"key":"e_1_3_3_3_1","doi-asserted-by":"publisher","DOI":"10.1111\/jvec.12258"},{"key":"e_1_3_3_4_1","first-page":"13","article-title":"The risk of exposure to Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, Babesia sp. and co-infections in Ixodes ricinus ticks on the territory of Niepo\u0142omice forest (southern Poland)","volume":"59","author":"Asman M","year":"2013","unstructured":"Asman M, , Nowak M. The risk of exposure to Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, Babesia sp. and co-infections in Ixodes ricinus ticks on the territory of Niepo\u0142omice forest (southern Poland). Ann Parasitol, 2013; 59:13\u201319.","journal-title":"Ann Parasitol"},{"key":"e_1_3_3_5_1","first-page":"413","article-title":"Anaplasma phagocytophilum in ticks from parks in the Emilia-Romagna region of northern Italy","volume":"48","author":"Aureli S","year":"2012","unstructured":"Aureli S, , Foley JE, , Galuppi R, , Rejmanek D, et al. Anaplasma phagocytophilum in ticks from parks in the Emilia-Romagna region of northern Italy. Vet Ital, 2012; 48:413\u2013423.","journal-title":"Vet Ital"},{"key":"e_1_3_3_6_1","first-page":"287","volume-title":"Ixodid Ticks\u2013Parasites and Vectors. St","author":"Balashov Yu S","year":"1998","unstructured":"Balashov Yu S. Ixodid Ticks\u2013Parasites and Vectors. 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