The infection of reintroduced ruminants – Bison bonasus and Alces alces – with Anaplasma phagocytophilum in northern Poland
-
Grzegorz Karbowiak
,
Bronislava Víchová
Abstract
The north-eastern part of Poland is considered an area of high risk for infection with tick-borne diseases, including with human granulocytic ehrlichiosis (HGE) agents. The etiological agent of HGE is Anaplasma phagocytophilum. As the animal reservoir for A. phagocytophilum in the environment serve the species from Cervidae and Bovidae families. European bison (Bison bonasus) and elk (Alces alces) are the big ruminant species, reintroduced to the forests of Middle Europe after many decades of absence. In the foci of zoonotic diseases they are able to play a role as natural reservoir to pathogens, however, their status as protected animals means their study has been rare and fragmentary. The studies of B. bonasus were conducted in Białowieża Primeval Forest and A. alces in Biebrza National Park. PCR amplifications were performed using primers amplifing the end of the groES gene, the intergenic spacer and approximately two-thirds of the groEL gene in the first round, and primers that span a 395-bp region of the groEL gene were used in the second round. The positive results were obtained in B. bonasus and A. alces, the prevalence of infection was 66.7 and 20.0%, respectively. Randomly selected samples were sequenced, sequences were compared with GenBank entries using Blast N2.2.13 and determined as A. phagocytophilum. The results presented herein are the first record of the presence of Anaplasma phagocytophilum in A. alces, and at the same time confirm the previous observations regarding the infection of B. bonasus with A. phagocytophilum.
References
Baldridge G.D., Scoles G.A., Burkhardt N.Y., Schloeder B., Kurtti T.J., Munderloh U.G. 2009. Transovarial transmission of Francisella-like endosymbionts and Anaplasma phagocytophilum variants in Dermacentor albipictus (Acari: Ixodidae). Journal of Medical Entomology, 46, 625-63210.1603/033.046.0330Search in Google Scholar
Bown K.J., Begon M., Bennett M., Woldehiwet Z., Ogden N.H. 2003. Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerging Infectious Diseases, 9, 63-7010.3201/eid0901.020169Search in Google Scholar
Chen S.M., Dumler J.S., Bakken J.S., Walker D.H. 1994. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. Journal of Clinical Microbiology, 32, 589-59510.1128/jcm.32.3.589-595.1994Search in Google Scholar
Dumler J.S., Barbet A.F., Bekker C.P.J., Dasch G.A., Palmer G.H., Ray S.C., Rikihisa Y., Rurangirwa F.R. 2001. 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 ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. International Journal of Systematic and Evolutionary Microbiology, 51, 2145-216510.1099/00207713-51-6-2145Search in Google Scholar
Gage K.L., Burkot T.R., Eisen R.J., Hayes E.B. 2008. Climate and vector-borne diseases. American Journal of Preventive Medicine, 35, 436-450. DOI: 10.1016/j.amepre.2008.08.03010.1016/j.amepre.2008.08.030Search in Google Scholar
Grzeszczuk A., Karbowiak G., Ziarko S., Kovalchuk O. 2006. The root-vole Microtus oeconomus (Pallas, 1776): a new potential reservoir of Anaplasma phagocytophilum. Vector Borne and Zoonotic Diseases, 6, 240-243. DOI: 10.1089/vbz.2006.6.24010.1089/vbz.2006.6.240Search in Google Scholar
Grzeszczuk A., Stańczak J., Kubica-Biernat B., Racewicz M., Kruminis- Łozowska W., Prokopowicz D. 2004a. Human anaplasmosis in north-eastern Poland: seroprevalence in humans and prevalence in Ixodes ricinus ticks. Annals of Agricultural and Environmental Medicine, 11, 99-103Search in Google Scholar
Grzeszczuk A., Ziarko S., Prokopowicz D., Radziwon P.M. 2004b. Zakażenie żubrow z Puszczy Białowieskiej bakteriami Anaplasma phagocytophilum. Medycyna Weterynaryjna, 60, 600-601Search in Google Scholar
Hapunik J., Vichova B., Karbowiak G., Wita I., Bogdaszewski M., Peťko B. 2011. Wild and farm breeding cervids infections with Anaplasma phagocytophilum. Annals of Agricultural and Environmental Medicine, 18, 73-77Search in Google Scholar
Holden K., Boothby J.T., Anand S., Massung R.F. 2003. Detection of Borrelia burgdorferi, Ehrlichia chaffeensis, and Anaplasma phagocytophilum in Ticks (Acari: Ixodidae) from a Coastal Region of California. Journal of Medical Entomology, 40, 534-53910.1603/0022-2585-40.4.534Search in Google Scholar
Humair P.F., Douet V., Moran Cadenas F., Schouls L.M., Van De Pol I., Gern L. 2007. Molecular identification of bloodmeal source in Ixodes rici nus ticks using 12S rDNA as a genetic marker. Journal of Medical Entomology, 44, 869-88010.1603/0022-2585(2007)44[869:MIOBSI]2.0.CO;2Search in Google Scholar
Karbowiak G., DemiaszkiewiczA.W., Pyziel A.M., Wita I., Moskwa B., Werszko J., Bień J., Goździk K., Lachowicz J., Cabaj W. 2014. The parasitic fauna of the European bison (Bison bonasus) (Linnaeus, 1758) and their impact on the conservation. Part 1. The summarising list of parasites noted. Acta Parasitologica, 59, 363-371. DOI: 10.2478/s11686-014-0252-010.2478/s11686-014-0252-0Search in Google Scholar
Karbowiak G., Slemenda S., Pieniazek N.J., Rychlik L., Stanko M., Sinski E., Wita I., Czaplinska U. 2004. Babesiosis of wild animals in Poland. In: Proceedings of the 9th European Multicolloquium of Parasitology, 18-23 July 2004, Valencia, Spain, 451Search in Google Scholar
Krasińska M., Krasiński Z. A. (Eds.). 2007. European bison. The Nature Monograph. Mammal Research Institute PAS, Białowieża, pp. 318Search in Google Scholar
Lotrič-Furlan S., Avsic-Zupanc T., Petrovec M., Nicholson W.L., Sumner J.W., Childs J.E., Strle F. 2001. Clinical and serological follow-up of patients with human granulocytic ehrlichiosis in Slovenia. Clinical and diagnostic laboratory immunology, 8, 899-903. DOI: 10.1128/CDLI.8.5.899-903.200110.1128/CDLI.8.5.899-903.2001Search in Google Scholar
Lotrič-Furlan S., Petrovec M., Zupanc T.A., Nicholson W.L., Sumner J.W., Childs J.E., Strle F. 1998. Human granulocytic ehrlichiosis in Europe: clinical and laboratory findings for four patients from Slovenia. Clinical Infectious Diseases, 27, 424-428. DOI: http://dx.doi.org/10.1086/51468310.1086/514683Search in Google Scholar PubMed
Morissette E., Massung R., Foley J.E., Alleman A.R., Foley P., Barbet A.F. 2009. Diversity of Anaplasma phagocytophilum strains, USA. Emerging Infectious Diseases, 15, 928-93110.3201/eid1506.081610Search in Google Scholar PubMed PubMed Central
Petrovec M., Bidovec A., Sumner J.W., Nicholson W.L., Childs J.E., Avšič-Županc T. 2002. Infection with Anaplasma phagocytophila in cervids from Slovenia: Evidence of two genotypic lineages. Wiener Klinische Wochenschrift, 114/13, 641-647Search in Google Scholar
Pucek Z., Raczyński J. (Eds.). 1983. Atlas of Polish Mammals. PWN, Warsaw, pp.188Search in Google Scholar
Silaghi C., Gilles J., Hohle M., Fingerle V., Just F.T., Pfister K. 2008. Anaplasma phagocytophilum infection in Ixodes ricinus, Bavaria, Germany. Emerging Infectious Diseases, 14, 972-97410.3201/eid1406.071095Search in Google Scholar PubMed PubMed Central
Stuen S., Akerstedt J., Bergstrom K., Handeland K. 2002. Antibodies to granulocytic Ehrlichia in moose, red deer, and roe deer in Norway. Journal of Wildlife Diseases, 38, 1-610.7589/0090-3558-38.1.1Search in Google Scholar PubMed
Sumner J.W., Nicholson W.L., Massung R.F. 1997. PCR amplifcation and comparison of nucleotide sequences from the groESL heat shock operon of Ehrlichia species. Journal of Clinical Microbiology, 35, 2087-209210.1128/jcm.35.8.2087-2092.1997Search in Google Scholar PubMed PubMed Central
Sytykiewicz H., Karbowiak G., Hapunik J., Szpechciński A., Supergan- Marwicz M., Goławska S., Sprawka I., Czerniewicz P. 2012. Molecular evidence of Anaplasma phagocytophilum and Babesia microti co-infections in Ixodes ricinus ticks in central-eastern region of Poland. Annals of Agricultural and Environmental Medicine, 19, 45-49Search in Google Scholar
Tylewska-Wierzbanowska S., Chmielewski T., Kondrusik M., Hermanowska- Szpakowicz T., Sawicki W., Sułek K. 2001. First cases of acute human granulocytic ehrlichiosis in Poland. European Journal Of Clinical Microbiology and Infectious Diseases, 20, 196-198. DOI:10.1007/s100960100464.10.1007/s100960100464Search in Google Scholar PubMed
Woldehiwet Z. 2006. Anaplasma phagocytophilum in ruminants in Europe. Annals of the New York Academy of Sciences, 1078: 446-460. DOI:10.1196/annals.1374.084 10.1196/annals.1374.084Search in Google Scholar PubMed
W. Stefański Institute of Parasitology, PAS
Articles in the same Issue
- Sperm transfer in monogenean (platyhelminth) parasites
- A survey for potentially zoonotic gastrointestinal parasites of dogs and pigs in Cambodia
- Tritrichomonas foetus infection in cat – first detection in Poland
- Association between immunoreactivity to Anisakis spp. antigens and high-risk pregnancy
- Stibarokris mariasi sp. nov. – a new quill mite species (Acariformes: Syringophilidae) parasitizing Puffinus pacificus (Gmelin) (Procellariidae) on Johnston Atoll
- Seroprevalence and correlates of Toxoplasma gondii infection in dairy cattle in northwest China
- Mites and internal parasites associated with the common dung beetle Geotrupes (Anoplotrupes) stercorosus (Hartmann in Scriba, 1791) in Poland
- New species of Cosmocercoides (Nematoda; Cosmocercidae) and other helminths in Gonocephalus liogaster (Squamata; Agamidae) from Peninsular Malaysia
- Cryptosporidium identification in HIV-Infected Humans. Experience from Kinshasa, the Democratic Republic of Congo
- The infection of reintroduced ruminants – Bison bonasus and Alces alces – with Anaplasma phagocytophilum in northern Poland
- Molecular studies on larvae of Pseudoterranova parasite of Trichiurus lepturus Linnaeus, 1758 and Pomatomus saltatrix (Linnaeus, 1766) off Brazilian waters
- Coexistence of Borrelia burgdorferi s.l. genospecies within Ixodes ricinus ticks from central and eastern Poland
- Molecular characterization of cystic echinococcosis: First record of G7 in Egypt and G1 in Yemen
- Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from southern Poland
- A new species of Cosmocerca (Nematoda: Cosmocercidae) and other helminths in Cyrtodactylus gubaot (Squamata: Gekkonidae) from the Philippines
- Alveolar echinococcosis: how knowledgeable are primary care physicians and pharmacists in the Franche-Comté region of France?
- Morphologic and molecular characteristics of Sarcocystis atraii n. sp. (Apicomplexa: Sarcocystidae) infecting the common coot (Fulica atra) from Egypt
- Auto-infection by Echinostoma spp. cercariae in Helisoma anceps
- Risk factors of occurrence of Toxoplasma gondii among horses in the state of Alagoas, Brazil
- Cardiopulmonary helminths in foxes from the Pyrenees
- Risk of soil-transmitted helminth infections on agritourism farms in central and eastern Poland
- Evaluating the Babesia bovis infection of cattle in China with enzyme-linked immunosorbent assay (ELISA)
- Production and preliminary evaluation of Trypanosoma evansi HSP70 for antibody detection in Equids
- Malondialdehyde; Lipid peroxidation plasma biomarker correlated with hepatic fibrosis in human Schistosoma mansoni infection
- A new species of the feather mite genus Tyrannidectes Mironov, 2008 (Acariformes: Proctophyllodidae) from tapaculos (Passeriformes: Rhinocryptidae) in Chile
- Recent study on canine vector-borne zoonoses in southern Slovakia – serologic survey
- Redescription of Paraleptus chiloscyllii Yin et Zhang, 1983 (Nematoda: Physalopteridae) from the Arabian carpetshark Chiloscyllium arabicum (Chondrichthyes: Hemiscylliidae) off Iraq
- A New Species of Ligophorus (Monogenea: Dactylogyridae) from the gills of the Flathead Mullet Mugil cephalus (Teleostei: Mugilidae) from Mexico
- Demodex mites as potential etiological factor in chalazion – a study in Poland
- First report of Schulzia travassosi (Nematoda, Trichostrongylina, Molineoidea) for amphibians of the Chaco region in Argentina and proposal of Oswaldocruzia melanostictusi nov. comb.
- First molecular identification of Ascocotyle (Phagicola) longa in its first intermediate host the mud snail Heleobia australis
- Dog’s genotype of Giardia duodenalis in human: first evidence in Europe
Articles in the same Issue
- Sperm transfer in monogenean (platyhelminth) parasites
- A survey for potentially zoonotic gastrointestinal parasites of dogs and pigs in Cambodia
- Tritrichomonas foetus infection in cat – first detection in Poland
- Association between immunoreactivity to Anisakis spp. antigens and high-risk pregnancy
- Stibarokris mariasi sp. nov. – a new quill mite species (Acariformes: Syringophilidae) parasitizing Puffinus pacificus (Gmelin) (Procellariidae) on Johnston Atoll
- Seroprevalence and correlates of Toxoplasma gondii infection in dairy cattle in northwest China
- Mites and internal parasites associated with the common dung beetle Geotrupes (Anoplotrupes) stercorosus (Hartmann in Scriba, 1791) in Poland
- New species of Cosmocercoides (Nematoda; Cosmocercidae) and other helminths in Gonocephalus liogaster (Squamata; Agamidae) from Peninsular Malaysia
- Cryptosporidium identification in HIV-Infected Humans. Experience from Kinshasa, the Democratic Republic of Congo
- The infection of reintroduced ruminants – Bison bonasus and Alces alces – with Anaplasma phagocytophilum in northern Poland
- Molecular studies on larvae of Pseudoterranova parasite of Trichiurus lepturus Linnaeus, 1758 and Pomatomus saltatrix (Linnaeus, 1766) off Brazilian waters
- Coexistence of Borrelia burgdorferi s.l. genospecies within Ixodes ricinus ticks from central and eastern Poland
- Molecular characterization of cystic echinococcosis: First record of G7 in Egypt and G1 in Yemen
- Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from southern Poland
- A new species of Cosmocerca (Nematoda: Cosmocercidae) and other helminths in Cyrtodactylus gubaot (Squamata: Gekkonidae) from the Philippines
- Alveolar echinococcosis: how knowledgeable are primary care physicians and pharmacists in the Franche-Comté region of France?
- Morphologic and molecular characteristics of Sarcocystis atraii n. sp. (Apicomplexa: Sarcocystidae) infecting the common coot (Fulica atra) from Egypt
- Auto-infection by Echinostoma spp. cercariae in Helisoma anceps
- Risk factors of occurrence of Toxoplasma gondii among horses in the state of Alagoas, Brazil
- Cardiopulmonary helminths in foxes from the Pyrenees
- Risk of soil-transmitted helminth infections on agritourism farms in central and eastern Poland
- Evaluating the Babesia bovis infection of cattle in China with enzyme-linked immunosorbent assay (ELISA)
- Production and preliminary evaluation of Trypanosoma evansi HSP70 for antibody detection in Equids
- Malondialdehyde; Lipid peroxidation plasma biomarker correlated with hepatic fibrosis in human Schistosoma mansoni infection
- A new species of the feather mite genus Tyrannidectes Mironov, 2008 (Acariformes: Proctophyllodidae) from tapaculos (Passeriformes: Rhinocryptidae) in Chile
- Recent study on canine vector-borne zoonoses in southern Slovakia – serologic survey
- Redescription of Paraleptus chiloscyllii Yin et Zhang, 1983 (Nematoda: Physalopteridae) from the Arabian carpetshark Chiloscyllium arabicum (Chondrichthyes: Hemiscylliidae) off Iraq
- A New Species of Ligophorus (Monogenea: Dactylogyridae) from the gills of the Flathead Mullet Mugil cephalus (Teleostei: Mugilidae) from Mexico
- Demodex mites as potential etiological factor in chalazion – a study in Poland
- First report of Schulzia travassosi (Nematoda, Trichostrongylina, Molineoidea) for amphibians of the Chaco region in Argentina and proposal of Oswaldocruzia melanostictusi nov. comb.
- First molecular identification of Ascocotyle (Phagicola) longa in its first intermediate host the mud snail Heleobia australis
- Dog’s genotype of Giardia duodenalis in human: first evidence in Europe
