{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T05:00:32Z","timestamp":1787029232080,"version":"build-2736575974"},"reference-count":51,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2021,4,11]],"date-time":"2021-04-11T00:00:00Z","timestamp":1618099200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Parasitic infections have a negative impact on the fecundity and survival of wild ruminants, particularly moose; however, despite being more susceptible to parasitic diseases than other wild cervids, they remain poorly examined in this regard. Therefore, the aim of the present study was to identify gastrointestinal and liver helminth species of the moose population in central Europe, assess the factors contributing to infection intensities and examine their impact on moose health. Abomasum, small intestine, caecum and liver samples were collected from 46 moose in Poland and evaluated for helminth parasite fauna and histopathological changes. Additionally, 289 moose fecal samples were analyzed for the presence of eggs, oocysts and larvae of parasites. In total, 19 parasite taxa were identified. The most prevalent were Mazamastrongylus dagestanica and Ostertagia antipini, which are typical nematodes of moose, together with Spiculopteragia boehmi and O. leptospicularis, characteristic also of other cervids. Parasite species diversity and abomasal parasitic infection intensity were higher in adult moose than in yearlings and calves. The numbers of histopathological lesions depended on the intensity of parasitic infections, and were most severe in the livers of moose infected with Parafasciolopsis fasciolaemorpha. The analysis of fecal samples revealed several regional differences in the levels of parasite eggs, oocysts and larvae shedding. Our findings indicate an accumulation of parasite infections over time in moose, which may be related to high environmental parasite pressure, possibly connected with high moose density and the presence of wetlands; they also serve as the most comprehensive study of moose parasites in central Europe to date.<\/jats:p>","DOI":"10.3390\/pathogens10040456","type":"journal-article","created":{"date-parts":[[2021,4,12]],"date-time":"2021-04-12T05:52:00Z","timestamp":1618206720000},"page":"456","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Gastrointestinal Helminths of a European Moose Population in Poland"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9490-8241","authenticated-orcid":false,"given":"Katarzyna","family":"Filip-Hutsch","sequence":"first","affiliation":[{"name":"Witold Stefa\u0144ski Institute of Parasitology PAS, Twarda 51\/55, 00-818 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4238-8360","authenticated-orcid":false,"given":"Micha\u0142","family":"Czopowicz","sequence":"additional","affiliation":[{"name":"Division of Veterinary Epidemiology and Economics, Institute of Veterinary Medicine, Warsaw University of Life Sciences\u2013SGGW, Nowoursynowska 159c, 02-776 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8675-5559","authenticated-orcid":false,"given":"Agnieszka","family":"Barc","sequence":"additional","affiliation":[{"name":"Veterinary Diagnostic Laboratory ALAB <i>bioscience<\/i>, Krucza 13, 05-090 Rybie, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aleksander W.","family":"Demiaszkiewicz","sequence":"additional","affiliation":[{"name":"Witold Stefa\u0144ski Institute of Parasitology PAS, Twarda 51\/55, 00-818 Warsaw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,4,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"937","DOI":"10.1046\/j.1365-2656.2002.00659.x","article-title":"The impact of gastrointestinal nematodes on wild reindeer: Experimental and cross-sectional studies","volume":"71","author":"Stien","year":"2002","journal-title":"J. Anim. Ecol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1007\/s13364-019-00423-8","article-title":"Factors affecting the spread of parasites in populations of wild European terrestrial mammals","volume":"64","year":"2019","journal-title":"Mammal Res."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/j.ijppaw.2014.12.005","article-title":"Endoparasites in a Norwegian moose (Alces alces) population - Faunal diversity, abundance and body condition","volume":"4","author":"Davidson","year":"2015","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"9006","DOI":"10.1073\/pnas.1201790109","article-title":"Parasite diversity and coinfection determine pathogen infection success and host fitness","volume":"109","author":"Johnson","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1111\/j.1365-2656.2010.01742.x","article-title":"Wildlife diseases: From individuals to ecosystems","volume":"80","author":"Tompkins","year":"2011","journal-title":"J. Anim. Ecol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"544","DOI":"10.1292\/jvms.17-0092","article-title":"Epizootic ofsarcoptic mange in raccoon dogs (Nyctereutes procyonoides) in relation to population density","volume":"80","author":"Sugiura","year":"2018","journal-title":"J. Vet. Med. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.1007\/s10980-020-01018-4","article-title":"Too hot to handle: Summer space use shift in a cold-adapted ungulate at the edge of its range","volume":"35","author":"Borowik","year":"2020","journal-title":"Landsc. Ecol."},{"key":"ref_8","first-page":"103","article-title":"Genetics, evolution and phylogeography of moose","volume":"40","author":"Hundertmark","year":"2004","journal-title":"Alces"},{"key":"ref_9","unstructured":"Ratkiewicz, M., Bereszy\u0144ski, A., G\u0142owaci\u0144ski, Z., Borkowska, A., Borkowski, J., Duda, N., Komenda, E., Raczy\u0144ski, J., Czajkowska, M., and Popczyk, B. (2011). Strategia Ochrony i Gospodarowania Populacj\u0105 \u0141osia w Polsce, NFO\u015aiGW. [1st ed.]."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1515\/ap-2016-0092","article-title":"Internal parasitic fauna of elk (Alces alces) in Poland","volume":"61","author":"Filip","year":"2016","journal-title":"Acta. Parasitol."},{"key":"ref_11","unstructured":"Wawrzyniak, P. (2016, January 5). Population dynamics, its impact upon the habitat and necessity of managament the moose (Alces alces) population in Poland. Proceedings of the Conference \u201cZarz\u0105dzanie Populacjami Zwierz\u0105t\u201d, Warsaw, Poland. (In Polish)."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"165","DOI":"10.7589\/2017-03-057","article-title":"Gastrointestinal Parasitic Infections in Dead or Debilitated Moose (Alces alces) in Sweden","volume":"54","author":"Grandi","year":"2018","journal-title":"J. Wildl. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/j.ijppaw.2020.02.007","article-title":"Patterns of parasite eggs, oocysts and larvae shedding by moose in the Biebrza marshland (NE Poland)","volume":"11","author":"Czopowicz","year":"2020","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.ijppaw.2020.10.008","article-title":"Sex-biased polyparasitism in moose (Alces alces) based on molecular analysis of faecal samples","volume":"13","author":"Borkowska","year":"2020","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_15","first-page":"259","article-title":"A contribution to the knowledge of Trichostrongylidae (Nematoda) from Alces alces (L.) of Finland","volume":"17","author":"Bylund","year":"1970","journal-title":"Acta Parasitol. Pol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"30","DOI":"10.3389\/fvets.2018.00030","article-title":"Transmission of Helminths between Species of Ruminants in Austria Appears More Likely to Occur than Generally Assumed","volume":"5","author":"Winter","year":"2018","journal-title":"Front. Vet. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2083","DOI":"10.1007\/s00436-012-3262-6","article-title":"Coccidia (Apicomplexa: Eimeriidae) of elk (Alces alces) in Poland","volume":"112","author":"Pyziel","year":"2013","journal-title":"Parasitol. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1007\/s10344-016-1037-6","article-title":"Does the blood-sucking nematode Ashworthius sidemi (Trichostrongylidae) cause deterioration of blood parameters in European bison (Bison bonasus)?","volume":"62","author":"Demiaszkiewicz","year":"2016","journal-title":"Eur. J. Wildl. Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/bs.apar.2016.02.022","article-title":"The Pathophysiology, Ecology and Epidemiology of Haemonchus contortus Infection in Small Ruminants","volume":"93","author":"Besier","year":"2016","journal-title":"Adv. Parasit."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1007\/s00436-002-0675-7","article-title":"Expansion of the Asiatic parasite Ashworthius sidemi (Nematoda, Trichostrongylidae) in wild ruminants in Polish territory","volume":"89","author":"Demiaszkiewicz","year":"2003","journal-title":"Parasitol. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1186\/s13071-014-0557-8","article-title":"Resurrection and redescription of Varestrongylus alces (Nematoda: Protostrongylidae), a lungworm of the Eurasian moose (Alces alces), with report on associated pathology","volume":"7","author":"Verocai","year":"2014","journal-title":"Parasit. Vectors"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.ijppaw.2020.11.007","article-title":"First report of a newly-described lungworm, Dictyocaulus cervi (Nematoda: Trichostrongyloidea), in moose (Alces alces) in central Europe","volume":"13","author":"Demiaszkiewicz","year":"2020","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_23","first-page":"20172610","article-title":"Predicting the effects of parasite co-infection across species boundaries","volume":"285","author":"Lello","year":"2018","journal-title":"Proc. Biol. Sci."},{"key":"ref_24","unstructured":"Kowalczyk, R., \u0141awreszuk, D., and W\u00f3jcik, J.M. (2010). Forming of European bison helminthfauna in Bia\u0142owie\u017ca Forest. European Bison Conservation in the Bia\u0142owie\u017ca Forest. Threats and Prospects of the Population Development, Zak\u0142ad Badania Ssak\u00f3w Polskiej Akademii Nauk. (In Polish)."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1186\/s13028-014-0059-x","article-title":"Gastrointestinal parasites in an isolated Norwegian population of wild red deer (Cervus elaphus)","volume":"56","author":"Davidson","year":"2014","journal-title":"Acta. Vet. Scand."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Samuel, W.M., Pybus, M.J., and Kocan, A.A. (2001). Gastrointestinal strongyles in wild ruminants. Parasitic Diseases of Wild Mammals, Iowa State University Press. [2nd ed.].","DOI":"10.1002\/9780470377000"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1625","DOI":"10.1098\/rspb.2002.2064","article-title":"The role of parasites in the dynamics of a reindeer population","volume":"169","author":"Albon","year":"2002","journal-title":"Proc. Biol. Sci."},{"key":"ref_28","first-page":"97","article-title":"The arthropod and helminth parasites of red deer (Cervus elaphus L) in New Zealand","volume":"5","author":"Andrews","year":"1964","journal-title":"Trans. R. Soc. N. Z."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.rvsc.2010.06.029","article-title":"Serum pepsinogen levels to monitor gastrointestinal nematode infections in cattle revisited","volume":"90","author":"Charlier","year":"2011","journal-title":"Res. Vet. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1002\/zoo.10059","article-title":"Importance of the wasting syndrome complex in captive moose (Alces alces)","volume":"21","author":"Clauss","year":"2002","journal-title":"Zoo. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1017\/S0022149X07850231","article-title":"Hepatic fibrosis and Fasciola hepatica infection in cattle","volume":"81","author":"Marcos","year":"2007","journal-title":"J. Helminthol."},{"key":"ref_32","first-page":"361","article-title":"Liver fluke disease (Fascioliasis): Epidemiology, economic impact and public health significance","volume":"22","author":"Saleha","year":"1991","journal-title":"Southeast Asian J. Trop. Med. Public Health"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1007\/s13364-013-0148-7","article-title":"Complex patterns of population genetic structure of moose, Alces alces, after recent spatial expansion in Poland revealed by sex-linked markers","volume":"58","author":"Czajkowska","year":"2013","journal-title":"Acta Theriol."},{"key":"ref_34","unstructured":"Apollonio, M., Andersen, R., and Putman, R. (2010). Ungulates and their management in Poland. European Ungulates and Their Management in the 21st Century, Cambridge University Press. [1st ed.]."},{"key":"ref_35","unstructured":"Chmielewski, T.J. (2009). Rezerwat Biosfery \u201cPolesie Zachodnie\u201d: Walory, Funkcjonowanie, Perspektywy Rozwoju, PPH Zapol. (In Polish)."},{"key":"ref_36","unstructured":"Andrzejewski, R. (2003). Klimat Puszczy Kampinoskiej. Kampinoski Park Narodowy. Tom 1. Przyroda Kampinoskiego Parku Narodowego, Kampinoski Park Narodowy. (In Polish)."},{"key":"ref_37","first-page":"1","article-title":"Studies on helminths and helminthiases in Cervidae II. The helminth fauna in Cervidae in Poland","volume":"14","year":"1966","journal-title":"Acta Parasitol. Pol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Peterson, R.L. (1955). A.T. A study of mandibular tooth wear as an index to age of moose. North American Moose, University of Toronto Press. [1st ed.].","DOI":"10.3138\/9781487578213"},{"key":"ref_39","first-page":"11","article-title":"A field technique for evaluating physical condition of deer","volume":"8","author":"Kistner","year":"1980","journal-title":"Wildl. Soc. Bull."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1007\/BF00009507","article-title":"Polymorphism in the Ostertagiinae (Lopez-Neyra, 1947) and comments on the systematics of these nematodes","volume":"32","year":"1995","journal-title":"Syst. Parasitol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/0304-4017(93)90046-P","article-title":"The systematics of nematodes that cause ostertagiasis in domestic and wild ruminants in North America: An update and a key to species","volume":"46","author":"Lichtenfels","year":"1993","journal-title":"Vet. Parasitol."},{"key":"ref_42","first-page":"107","article-title":"A massive invasion of Parafasciolopsis fasciolaemorpha in elk (Alces alces) in Lublin Province, Poland","volume":"62","author":"Filip","year":"2016","journal-title":"Ann. Parasitol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"549","DOI":"10.2478\/jvetres-2019-0068","article-title":"First description of histopathological lesions associated with a fatal infection of moose (Alces alces) with the liver fluke Parafasciolopsis fasciolaemorpha Ejsmont, 1932","volume":"63","author":"Hutsch","year":"2019","journal-title":"J. Vet. Res."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Taylor, M.A. (2015). Coop, R.L.; Wall, R.L. Veterinary Parasitology, Wiley-Blackwell. [4th ed.].","DOI":"10.1002\/9781119073680"},{"key":"ref_45","unstructured":"Ziomko, I., and Cencek, T. (1999). Inwazje Paso\u017cytnicze Zwierz\u0105t Gospodarskich, Drukarnia Piotra W\u0142odarskiego. [1st ed.]. (In Polish)."},{"key":"ref_46","unstructured":"Bowman, D.D. (2009). Georgis\u2019 Parasitology for Veterinarians, Saunders. [9th ed.]."},{"key":"ref_47","first-page":"331","article-title":"The first record of Elaphostrongylus alces larvae in moose in Poland and theirdevelopment to invasive stage","volume":"53","author":"Goliszewska","year":"2007","journal-title":"Wiad. Parazytol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1139\/z97-168","article-title":"Olsson, I.M.C.; Steen, M.; Gajadhar, A. Extra-mammalian larval stages of Elaphostrongylus alces (Nematoda: Protostrongylidae), a parasite of moose (Alces alces) in Fennoscandia","volume":"76","author":"Lankester","year":"2011","journal-title":"Can. J. Zool"},{"key":"ref_49","unstructured":"Altman, D.G., Machin, D., Bryant, T.N., and Gardner, M.J. (2000). Statistics with Confidence, BMJ Books."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.tjem.2018.08.001","article-title":"User\u2019s guide to correlation coefficients","volume":"18","author":"Akoglu","year":"2018","journal-title":"Turk. J. Emerg. Med."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1186\/s13071-018-2958-6","article-title":"Chovancov\u00e1, G.; Rehbein, S. Host specificity and species diversity of the Ostertagiinae Lopez-Neyra, 1947 in ruminants: A European perspective","volume":"11","author":"Kowal","year":"2018","journal-title":"Parasit. Vectors"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/4\/456\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T13:59:25Z","timestamp":1760363965000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/4\/456"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,4,11]]},"references-count":51,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2021,4]]}},"alternative-id":["pathogens10040456"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10040456","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,4,11]]}}}