A frequent roundworm Baylisascaris transfuga in overpopulated brown bears (Ursus arctos) in Slovakia: a problem worthy of attention
-
Gabriela Štrkolcová
,
Mária Goldová
Abstract
The genus Baylisascaris (order Ascaridida) includes numerous relatively host-specific nematodes, which are common in intestines of wild mammals. Some of them may have impact on veterinary and public health, as their larvae have the potential to cause visceral, ocular, and/or neural larva migrans in a wide range of mammals, birds, and humans. Baylisascaris transfuga is a parasite occurring in a range of bear species throughout the world. We present the current data on B. transfuga occurrence in brown bears from a relatively restricted territory of the Poľana Protected Landscape Area in Central Slovakia, obtained by traditional methods (faecal examination, morphology). Species affiliation was confirmed by employing molecular markers generating nuclear 28S and mitochondrial cox1 sequences in adult worms. Based on 17 examined samples (15 excrements and two intestines of young bear females), the occurrence of B. transfuga in the surveyed area was assessed as 52.9%. Both bear females were infected with adult and juvenile worms. Due to the high density of bears in the locality, the high infection rate with ascarids, and the huge number of eggs produced by the parasites, it is apparent that the respective environment, including the inhabited areas, might be markedly contaminated by Baylisascaris eggs. The ability of B. transfuga to serve as a zoonotic agent has not been unambiguously proved; however, this attribute should be considered and subjected to further research.
Acknowledgements
The authors are highly indebted to Prof. L. Paule and Assoc. Prof. D. Rajský, Technical University in Zvolen, Slovakia, for the information about the local bear density and raccoon occurrence in various Slovak regions. The study was supported by the grants of the State Agency VEGA No. 1/0455/15 and No. 2/0162/17, and the Internal Grant Agency UVLF 01/2016.
References
Bauer C. 2013. Baylisascariosis–infections of animals and humans with ‘unusual’ roundworms. Veterinary Parasitology, 193, 404–412. 10.1016/j.vetpar.2012.12.036Search in Google Scholar PubMed
Blouin M.S., Yowell C.A., Courtney C.H., Dame J.B. 1998. Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Molecular Biology and Evolution, 15, 1719–172710.1093/oxfordjournals.molbev.a025898Search in Google Scholar PubMed
Borka-Vitalis L., Domokos C., Foldvari G., Majoros G. 2017. Endoparasites of brown bears in Eastern Transylvania, Romania. Ursus, 28, 20–30. 10.2192/URSUS-D-16-00015.1Search in Google Scholar
De Ambrogi M., Aghazadeh M., Hermosilla C., Huber D., Majnaric D., Reljic S. et al. 2011. Occurrence of Baylisascaris transfuga in wild populations of European brown bears (Ursus arctos) as identified by a new PCR method. Veterinary Parasitology, 179, 272–276. 10.1016/j.vetpar.2011.02.025Search in Google Scholar PubMed
Finnegan S. 2009. Seasonal dynamics in the prevalence of Baylisascaris transfuga ova in the faeces of the brown bear (Ursus arctos) in Slovakia. Diploma Thesis, University of Veterinary Medicine and Pharmacy in Košice, SlovakiaSearch in Google Scholar
Foster G.W., Cunningham M.W., Kinsella J.M., Forrester D.J. 2004. Parasitic helminths of black bear cubs (Ursus americanus) from Florida. Journal of Parasitology, 90, 173–175. 10.1645/GE-127RSearch in Google Scholar PubMed
Franssen F., Xie K., Sprong H., Van der Giessen J. 2013. Molecular analysis of Baylisascaris columnaris revealed mitochondrial and nuclear polymorphisms. Parasite & Vectors, 6, 124. 10.1186/1756-3305-6-124Search in Google Scholar PubMed PubMed Central
Gavin PJ., Kazacos K.R., Shulman S. 2005. Baylisascariasis. Clinical Microbiology Reviews, 18. 703–718. 10.1128/CMR.18.4.703-718.2005Search in Google Scholar PubMed PubMed Central
Goldová M., Ciberej J., Rigg R. 2003. Medveď hnedý (Ursus arctos) a parazitarne zoonozy. (Brown bear (Ursus arctos) and parasitic zoonoses). Folia Venatoria, 33, 123–127. (In Slovak)Search in Google Scholar
Guerrero R., Castellanos A. 2016. First record of Baylisascaris transfuga (Nematoda: Ascarididae) in an Anden Bear (Tremarctos ornatus) in Ecuador. International Bear News, 25. IBA website: www.bearbiology.orgSearch in Google Scholar
Huff D.S., Neafie R.C., Binder M.J., De Leon G.A., Brown L.W., Kazacos K.R. 1984. Case 4. The first fatal Baylisascaris infection in humans: an infant with eosinophilic meningoencephalitis. Pediatric Pathology, 2, 345–35210.3109/15513818409022268Search in Google Scholar PubMed
Kazacos K.R. 2016. Baylisascaris Larva Migrans: U.S. Geological Survey Circular 1412, 122 pp. 3 appendixes, http://www.arlis.org/docs/vol1/M/946142348.pdf10.3133/cir1412Search in Google Scholar
Krištofík J., Danko Š. 2012. Cicavce Slovenska. Rozšírenie, bionómia a ochrana (Mammals of Slovakia. Distribution, bionomy and protection). Veda, Bratislava, 712 pp. (In Slovak)Search in Google Scholar
Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H. et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948. 10.1093/bioinformatics/btm404Search in Google Scholar PubMed
Lenko P., Tajboš P., Humený M., Celer S., Zwijacz–Kozica T., Zięba F. et al. 2014. Problematika a súčasný stav medveďa hnedého v Tatrách (Problems and the current state of the brown bear in the Tatras). OZ Les, Správa Tatranského národného parku, Tatranská Štrba, 91 pp. (In Slovak with English summary)Search in Google Scholar
Li Y., Niu L., Wang Q., Zhang Z., Chen Z., Gu X. et al. 2012. Molecular characterization and phylogenetic analysis of ascarid nematodes from twenty-one species of captive wild mammals based on mitochondrial and nuclear sequences. Parasitology, 139, 1329–1938. 10.1017/S003118201200056XSearch in Google Scholar PubMed
Major P., Molnár L., Štofik J., Goldová M. 2009. Parasitofauna medveďa hnedého v NP Poloniny (Parasitofauna of the brown bear (Ursus arctos) in Poloniny National Park). In: Škola – veda – prax I. September 24, 2009, University of Veterinary Medicine and Pharmacy in Košice, Slovakia, 318–322. (In Slovak)Search in Google Scholar
Matoff K., Komandarev S. 1965. Comparative studies on the migration of the larvae Toxascaris leonina and Toxascaris transfuga. Parasitology Research, 25, 538–55510.1007/BF00259600Search in Google Scholar
Manual of Veterinary Laboratory Methods. 1989. Ministry of Agriculture, Fisheries and Food. Reference Book 418. Her Majesty’s Stationary Office, London, UKSearch in Google Scholar
Moudgil A.D., Singla L.D., Singh M.P. 2014. First report on molecular identification and fenbendazole resistance against Baylisascaris transfuga infection in Melursus ursinus (sloth bear). Helminthologia, 51, 262–268. 10.2478/s11687-014-0239-2Search in Google Scholar
Papini R., Casarosa L. 1994. A report on the pathology of Baylisascaris transfuga (Ascarididae: Nematoda) for mice. Revue de Médecine Vétérinaire (Toulouse), 145, 949–952Search in Google Scholar
Papini R., Renzoni G., Lo Piccolo S., Casarosa L. 1996. Ocular larva migrans and histopathological lesions in mice experimentally infected with Baylisascaris transfuga embryonated eggs. Veterinary Parasitology, 61, 315–32010.1016/0304-4017(95)00825-XSearch in Google Scholar PubMed
Paule L., Krajmerová D., Bakan J. 2016a. Kolik medvědů žije na Slovensku? (How many bears live in Slovakia?) Svět myslivosti 3, 17, 14–17. (In Czech)Search in Google Scholar
Paule L., Krajmerová D., Bakan J., Slivková V. 2016b. Odhad veľkosti populácie medveďa hnedého na Slovensku na základe genetických analyz (Estimation of brown bear population size in Slovakia based on genetic analyses). Chapter in the book: Conservation and management of large carnivores in Slovakia, Štátna ochrana prírody SR, Banská Bystrica, Editors: Lešová A, Antal V, pp.73–84. (In Slovak)Search in Google Scholar
Sapp S.G.H., Gupta P., Martin M.K., Murray M.H., Niedringhaus K.D., Pfaff M.A. et al. 2017. Beyond the raccoon roundworm: The natural history of non-raccoon Baylisascaris species in the New World. International Journal for Parasitology: Parasites and Wildlife, 6, 85–99. 10.1016/j.ijppaw.2017.04.003Search in Google Scholar PubMed PubMed Central
Sato H., Matsuo K., Osanai A., Kamiya H., Akao N., Owaki S. et al. 2004. Larva migrans by Baylisascaris transfuga: Fatal neurological diseases in Mongolian jirds, but not in mice. Journal of Parasitology, 90, 774–781. 10.1645/GE-3330Search in Google Scholar PubMed
Sato H., Une Y., Kawakami S., Saito E., Kamiya H., Akao N. et al. 2005. Fatal Baylisascaris larva migrans in a colony of Japanese macaques kept by a safari-style zoo in Japan. Journal of Parasitology 91, 716–719. 10.1645/GE-3374RNSearch in Google Scholar PubMed
Schaul J.C. 2006. Baylisascaris transfuga in captive and free-ranging populations of bears (Family: Ursidae). PhD Thesis, Ohio State University, USA. https://etd.ohiolink.edu/rws_etd/document/get/osu1163172292/inlineSearch in Google Scholar
Servheen C. 1990. The status and conservation of the bears of the world. International Conference on Bear Research and Management, Monograph Series No. 2, 1–32Search in Google Scholar
Soulsby J.F.A. 1986. Helminths, Arthropods and Protozoa of Domesticated Animals. Bailiére-Tindall, London, UK, 809 pp.Search in Google Scholar
Szczepaniak K., Listos P., Lopuszynski W., Skrzypek T., Kazimierczak W. 2012. Granulomatous peritonitis in a European brown bear caused by Baylisascaris transfuga. Journal of Wildlife Diseases 48, 517–519. 10.7589/0090-3558-48.2.517Search in Google Scholar PubMed
Testini G., Papini R., Lia R.P., Parisi A., Dantas-Torres F., Traversa D. et al. 2011. New insights into the morphology, molecular characterization and identification of Baylisascaris transfuga (Ascaridida, Ascarididae). Veterinary Parasitology 175, 97–102. 10.1016/j.vetpar.2010.09.017Search in Google Scholar PubMed
VisserM.H., van der Giessen J.W.B., Franssen F., van Knapen F., Overgaauw P.A.M. 2015. Survey of Baylisascaris sp. in zoo-animals in the Netherlands. Master Thesis, Faculty of Veterinary Medicine Theses, Utrecht University, NetherlandsSearch in Google Scholar
Waits L., Taberlet P., Swenson J.E., Sandegren F., Franzén R. 2000. Nuclear DNA microsatellite analysis of genetic diversity and gene flow in the Scandinavian brown bear (Ursus arctos). Molecular Ecology, 9, 421–431. 10.1046/j.1365-294x.2000.00892.xSearch in Google Scholar PubMed
Xie Y., Zhang Z., Wang C., Lan J., Li Y., Chen Z. et al. 2011. Complete mitochondrial genomes of Baylisascaris schroederi, Baylisascaris ailuri and Baylisascaris transfuga from giant panda, red panda and polar bear. Gene, 482, 59–67. 10.1016/j.gene.2011.05.004Search in Google Scholar PubMed
© 2018 W. Stefański Institute of Parasitology, PAS
Articles in the same Issue
- Invited Paper
- Ultrastructure of digenean trematode eggs (Platyhelminthes: Neoophora): A review emphasizing new comparative data on four European Microphalloidea
- Phylogeny and cocoon production in the parasitic leech Myzobdella lugubris Leidy, 1851 (Hirudinidae, Piscicolidae)
- Parasites in stray dogs from Italy: prevalence, risk factors and management concerns
- A serological study of antibodies to Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in the sera of healthy individuals collected two decades apart
- Changes in the incidence of intestinal giardiosis in Mexican population during five years (2011-2015)
- Molecular target analysis of stearoyl-CoA desaturase genes of protozoan parasites
- Molecular and morphological characterisation of Rhabdias picardiae Junker, Lhermitte-Vallarino et Bain, 2010 (Nematoda: Rhabdiasidae) from Delaland’s River Frog, Amietia delalandii (Duméril et Bibron, 1841) (Amphibia: Pyxicephalidae) in South Africa
- Scanning electron microscopy study of Strabax monstrosus von Nordmann, 1864 (Copepoda: Chondracanthidae) from Tunisian waters and histopathological study of its effects on host
- Characterization of phosphate transporter(s) and understanding their role in Leishmania donovani parasite
- Two nematode species from freshwater and marine fishes in Thailand, including Ascarophis scatophagi sp. nov. (Cystidicolidae) from Scatophagus argus (Scatophagidae)
- Metazoan parasite fauna of migrating common garfish, Belone belone (L.), in the Baltic Sea
- Measurement of binding strength between prey proteins interacting with Toxoplasma gondii SAG1 and SAG2 using isothermal titration calorimetry (ITC)
- Asymmetric peptidomimetics containing L-tartaric acid core inhibit the aspartyl peptidase activity and growth of Leishmania amazonensis promastigotes
- Transcriptional analysis of immune-relevant genes in the mucus of Labeo rohita, experimentally infected with Argulus siamensis
- Prevalence of endoparasitic infections of birds in zoo gardens in Serbia
- Contamination of swimming pools and hot tubs biofilms with Acanthamoeba
- Morphological and molecular characterization of Seuratascaris numidica (Seurat, 1917) (Ascaridida: Ascarididae)
- Nematode Thelazia callipaeda is spreading across Europe. The first survey of red foxes from Slovakia
- A frequent roundworm Baylisascaris transfuga in overpopulated brown bears (Ursus arctos) in Slovakia: a problem worthy of attention
- Nematode parasites of Duttaphrynus stomaticus (Lutken, 1864) (Amphibia: Anura) with description of a new species of Rhabdias Stiles and Hassall, 1905 (Nematoda: Rhabdiasidae) from Dehradun (Uttarakhand), India
- Molecular and serological investigation of infectious diseases in captive and free-range crab-eating fox (Cerdocyon thous – Linnaeus, 1776) from northeastern Brazil
- A new species of Aplectana (Nematoda, Cosmocercidae) in Goniurosaurus bawanglingensis (Squamata, Eublepharidae), from Hainan Province, China
- Syphacia muris infection in rats attenuates colorectal carcinogenesis through oxidative stress and gene expression alterations. Implications for modulatory effects by Bryostatin-1
- Research Note
- The first case of Leporacarus gibbus infestation in a rabbit from Poland
- Research Note
- Pathological and molecular studies of the renal trematode Paratanaisia bragai in Indian peafowls (Pavo cristatus)
Articles in the same Issue
- Invited Paper
- Ultrastructure of digenean trematode eggs (Platyhelminthes: Neoophora): A review emphasizing new comparative data on four European Microphalloidea
- Phylogeny and cocoon production in the parasitic leech Myzobdella lugubris Leidy, 1851 (Hirudinidae, Piscicolidae)
- Parasites in stray dogs from Italy: prevalence, risk factors and management concerns
- A serological study of antibodies to Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in the sera of healthy individuals collected two decades apart
- Changes in the incidence of intestinal giardiosis in Mexican population during five years (2011-2015)
- Molecular target analysis of stearoyl-CoA desaturase genes of protozoan parasites
- Molecular and morphological characterisation of Rhabdias picardiae Junker, Lhermitte-Vallarino et Bain, 2010 (Nematoda: Rhabdiasidae) from Delaland’s River Frog, Amietia delalandii (Duméril et Bibron, 1841) (Amphibia: Pyxicephalidae) in South Africa
- Scanning electron microscopy study of Strabax monstrosus von Nordmann, 1864 (Copepoda: Chondracanthidae) from Tunisian waters and histopathological study of its effects on host
- Characterization of phosphate transporter(s) and understanding their role in Leishmania donovani parasite
- Two nematode species from freshwater and marine fishes in Thailand, including Ascarophis scatophagi sp. nov. (Cystidicolidae) from Scatophagus argus (Scatophagidae)
- Metazoan parasite fauna of migrating common garfish, Belone belone (L.), in the Baltic Sea
- Measurement of binding strength between prey proteins interacting with Toxoplasma gondii SAG1 and SAG2 using isothermal titration calorimetry (ITC)
- Asymmetric peptidomimetics containing L-tartaric acid core inhibit the aspartyl peptidase activity and growth of Leishmania amazonensis promastigotes
- Transcriptional analysis of immune-relevant genes in the mucus of Labeo rohita, experimentally infected with Argulus siamensis
- Prevalence of endoparasitic infections of birds in zoo gardens in Serbia
- Contamination of swimming pools and hot tubs biofilms with Acanthamoeba
- Morphological and molecular characterization of Seuratascaris numidica (Seurat, 1917) (Ascaridida: Ascarididae)
- Nematode Thelazia callipaeda is spreading across Europe. The first survey of red foxes from Slovakia
- A frequent roundworm Baylisascaris transfuga in overpopulated brown bears (Ursus arctos) in Slovakia: a problem worthy of attention
- Nematode parasites of Duttaphrynus stomaticus (Lutken, 1864) (Amphibia: Anura) with description of a new species of Rhabdias Stiles and Hassall, 1905 (Nematoda: Rhabdiasidae) from Dehradun (Uttarakhand), India
- Molecular and serological investigation of infectious diseases in captive and free-range crab-eating fox (Cerdocyon thous – Linnaeus, 1776) from northeastern Brazil
- A new species of Aplectana (Nematoda, Cosmocercidae) in Goniurosaurus bawanglingensis (Squamata, Eublepharidae), from Hainan Province, China
- Syphacia muris infection in rats attenuates colorectal carcinogenesis through oxidative stress and gene expression alterations. Implications for modulatory effects by Bryostatin-1
- Research Note
- The first case of Leporacarus gibbus infestation in a rabbit from Poland
- Research Note
- Pathological and molecular studies of the renal trematode Paratanaisia bragai in Indian peafowls (Pavo cristatus)
