Abstract
In Western Europe, the Echinococcus multilocularis lifecycle is predominantly sylvatic, typically involving red foxes (Vulpes vulpes) as the main definitive hosts with Microtus spp. and Arvicola spp. as intermediate hosts. During a 4-year surveillance study (2012–2015), Danish red foxes and raccoon dogs (n = 1345) were examined for E. multilocularis. Moreover, 134 insectivores and rodents collected in South Jutland during spring and summer 2016 were examined for the presence of metacestodes. The sedimentation and counting technique and molecular typing were used to identify E. multilocularis infections in the carnivores, while the rodent livers were examined macro- and microscopically for parasite lesions. Following morphological identification of E. multilocularis adult worms, the identity was verified by sequence analysis of the 12S rRNA gene in most cases (n = 13). Echinococcus multilocularis infection was demonstrated in 19 red foxes (Vulpes vulpes) originating from only two specific areas of South Jutland, namely Højer and Grindsted, and in two raccoon dogs (Nyctereutes procyonoides), originating from Højer. In Højer, 28.5% (CI 95% 11.7–45.3) of the examined red foxes were E. multilocularis positive per year. Moreover, positive red foxes were identified each year from 2012 to 2015, while E. multilocularis positive red foxes were only identified in Grindsted in 2013 (4.0%) and 2014 (6.4%). In contrast, all collected rodents were negative for E. multilocularis. We conclude that E. multilocularis is locally endemic in South Jutland with a high local prevalence in Højer.
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References
(2016) Reconsider timing of E. multilocularis treatment, suggests EFSA. Vet Rec 178:79
Al-Sabi MNS, Chriél M, Jensen TH, Enemark HL (2013) Endoparasites of the raccoon dog (Nyctereutes procyonoides) and the red fox (Vulpes vulpes) in Denmark 2009–2012—a comparative study. Int J Parasitol Parasites Wildl 2:144–151. https://doi.org/10.1016/j.ijppaw.2013.04.001
Al-Sabi MNS, Halasa T, Kapel CMO (2014) Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark. Acta Parasitol 59:98–107. https://doi.org/10.2478/s11686-014-0214-6
Baggøe HJ, Jensen TS (2007) Dansk Pattedyratlas. Gyldendal
Bagrade G, Deksne G, Ozoliņa Z, Howlett SJ, Interisano M, Casulli A, Pozio E (2016) Echinococcus multilocularis in foxes and raccoon dogs: an increasing concern for Baltic countries. Parasit Vectors 9:615. https://doi.org/10.1186/s13071-016-1891-9
Beerli O, Guerra D, Baltrunaite L, Deplazes P, Hegglin D (2017) Microtus arvalis and Arvicola scherman: key players in the Echinococcus multilocularis life cycle. Front Vet Sci 4:216. https://doi.org/10.3389/fvets.2017.00216
Berke O, Romig T, von Keyserlingk M (2008) Emergence of Echinococcus multilocularis among red foxes in northern Germany, 1991-2005. Vet Parasitol 155:319–322. https://doi.org/10.1016/j.vetpar.2008.05.017
Bouwknegt M, Devleesschauwe B, Graham H et al (2018) Prioritisation of food-borne parasites in Europe, 2016. Euro Surveill 23:1–11. https://doi.org/10.2807/1560-7917.ES.2018.23.9.17-00161
Bružinskaitė-Schmidhalter R, Šarkūnas M, Malakauskas A et al (2012) Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania. Parasitology 139:120–127. https://doi.org/10.1017/S0031182011001715
Davidson RK, Romig T, Jenkins E, Tryland M, Robertson LJ (2012) The impact of globalisation on the distribution of Echinococcus multilocularis. Trends Parasitol 28:239–247. https://doi.org/10.1016/j.pt.2012.03.004
Denzin N, Schliephake A, Froehlich A et al (2014) On the move? Echinococcus multilocularis in red foxes of Saxony-Anhalt (Germany). Transbound Emerg Dis 61:239–246. https://doi.org/10.1111/tbed.12026
Eckert J, Gemmell MA, Meslin F, Pawlowski ZS (2001) WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. OIE, France
Enemark HL, Al-Sabi MN, Knapp J et al (2013) Detection of a high-endemic focus of Echinococcus multilocularis in red foxes in southern Denmark, January 2013. Euro Surveill 18:2–5
European Food Safety Authority EFS (2015) EFSA journal. European Food Safety Authority
Giraudoux P, Raoul F, Afonso E et al (2013) Transmission ecosystems of Echinococcus multilocularis in China and Central Asia. Parasitology 140:1655–1666. https://doi.org/10.1017/S0031182013000644
Guerra D, Hegglin D, Bacciarini L et al (2014) Stability of the southern European border of Echinococcus multilocularis in the Alps: evidence that Microtus arvalis is a limiting factor. Parasitology 141:1593–1602. https://doi.org/10.1017/S0031182014000730
Hanosset R, Saegerman C, Adant S, Massart L, Losson B (2008) Echinococcus multilocularis in Belgium: prevalence in red foxes (Vulpes vulpes) and in different species of potential intermediate hosts. Vet Parasitol 151:212–217. https://doi.org/10.1016/j.vetpar.2007.09.024
Hofer S, Gloor S, Müller U et al (2000) High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zürich, Switzerland. Parasitology 120:135–142
Isaksson M, Hagstrom A, Armua-Fernandez MT et al (2014) A semi-automated magnetic capture probe based DNA extraction and real-time PCR method applied in the Swedish surveillance of Echinococcus multilocularis in red fox (Vulpes vulpes) faecal samples. Parasit Vectors 7:583. https://doi.org/10.1186/s13071-014-0583-6
Kapel CMO, Torgerson PR, Thompson RCA, Deplazes P (2006) Reproductive potential of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and cats. Int J Parasitol 36:79–86. https://doi.org/10.1016/j.ijpara.2005.08.012
Knapp J, Bart JM, Glowatzki ML, Ito A, Gerard S, Maillard S, Piarroux R, Gottstein B (2007) Assessment of use of microsatellite polymorphism analysis for improving spatial distribution tracking of Echinococcus multilocularis. J Clin Microbiol 45:2943–2950. https://doi.org/10.1128/JCM.02107-06
Laurimaa L, Süld K, Moks E, Valdmann H, Umhang G, Knapp J, Saarma U (2015) First report of the zoonotic tapeworm Echinococcus multilocularis in raccoon dogs in Estonia, and comparisons with other countries in Europe. Vet Parasitol 212:200–205. https://doi.org/10.1016/j.vetpar.2015.06.004
Liccioli S, Giraudoux P, Deplazes P, Massolo A (2015) Wilderness in the “city” revisited: different urbes shape transmission of Echinococcus multilocularis by altering predator and prey communities. Trends Parasitol 31:297–305. https://doi.org/10.1016/j.pt.2015.04.007
Lind EO, Juremalm M, Christensson D et al (2011) First detection of Echinococcus multilocularis in Sweden, February to March 2011. Euro Surveill 16:4–6
Meia J-S, Weber J-M (1995) Home ranges and movements of red foxes in central Europe: stability despite environmental changes. Can J Zool 73:1960–1966. https://doi.org/10.1139/z95-230
Oksanen A, Siles-Lucas M, Karamon J, Possenti A, Conraths FJ, Romig T, Wysocki P, Mannocci A, Mipatrini D, la Torre G, Boufana B, Casulli A (2016) The geographical distribution and prevalence of Echinococcus multilocularis in animals in the European Union and adjacent countries: a systematic review and meta-analysis. Parasit Vectors 9:519. https://doi.org/10.1186/s13071-016-1746-4
Pleydell DRJ, Raoul F, Tourneux F, Danson FM, Graham AJ, Craig PS, Giraudoux P (2004) Modelling the spatial distribution of Echinococcus multilocularis infection in foxes. Acta Trop 91:253–265. https://doi.org/10.1016/j.actatropica.2004.05.004
Romig T, Thoma D, Weible A-K (2006) Echinococcus multilocularis—a zoonosis of anthropogenic environments? J Helminthol 80:207–212. https://doi.org/10.1079/JOH2006347
Romig T, Deplazes P, Jenkins D et al (2017) Ecology and life cycle patterns of Echinococcus species. Adv Parasitol 95:213–314. https://doi.org/10.1016/bs.apar.2016.11.002
Saeed I, Maddox-Hyttel C, Monrad J, Kapel CMO (2006) Helminths of red foxes (Vulpes vulpes) in Denmark. Vet Parasitol 139:168–179. https://doi.org/10.1016/j.vetpar.2006.02.015
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schwarz S, Sutor A, Staubach C, Mattis R, Tackmann K, Conraths FJ (2011) Estimated prevalence of Echinococcus multilocularis in raccoon dogs Nyctereutes procyonoides in northern Brandenburg, Germany. Curr Zool 57:655–661. https://doi.org/10.1093/czoolo/57.5.655
Statens Serum Institute (2017) Bændelorm påvist på Statens Serum Institut i perioden 2005–2015. In: EPI-NYT. http://www.ssi.dk/Aktuelt/Nyhedsbreve/EPI-NYT/2017/Uge 4–2017.aspx. Accessed 12 Jun 2017
Staubach C, Hoffmann L, Schmid VJ, Ziller M, Tackmann K, Conraths FJ (2011) Bayesian space-time analysis of Echinococcus multilocularis-infections in foxes. Vet Parasitol 179:77–83. https://doi.org/10.1016/j.vetpar.2011.01.065
Stefanic S, Shaikenov BS, Deplazes P et al (2004) Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (“sheep strain”) in naturally infected dogs. Parasitol Res 92:347–351. https://doi.org/10.1007/s00436-003-1043-y
Stieger C, Hegglin D, Schwarzenbach G et al (2002) Spatial and temporal aspects of urban transmission of Echinococcus multilocularis. Parasitology 124:631–640. https://doi.org/10.1017/S0031182002001749
Takeuchi-Storm N, Woolsey ID, Jensen PM, Fredensborg BL, Pipper CB, Kapel CMO (2015) Predictors of Echinococcus multilocularis prevalence in definitive and intermediate hosts: a meta-analysis approach. J Parasitol 101:297–303. https://doi.org/10.1645/14-645.1
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Torgerson PR, Schweiger A, Deplazes P, Pohar M, Reichen J, Ammann RW, Tarr PE, Halkik N, Müllhaupt B (2008) Alveolar echinococcosis: from a deadly disease to a well-controlled infection. Relative survival and economic analysis in Switzerland over the last 35 years. J Hepatol 49:72–77. https://doi.org/10.1016/j.jhep.2008.03.023
Trachsel D, Deplazes P, Mathis A (2007) Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134:911. https://doi.org/10.1017/S0031182007002235
Wilson DE, Reeder DM (2005) Mammal species of the world: a taxonomic and geographic reference. Online database from Smithson. Natl. Museum Nat. Hist. http//vertebrates.si.edu/msw/mswCFApp/msw/index.cfm 2142
Winge H (1908) Pattedyr - Bind 5 i Danmarks fauna. G.E.C. Gads Forlag, Copenhagen, Denmark
Woolsey ID, Bune NET, Jensen PM, Deplazes P, Kapel CMO (2015) Echinococcus multilocularis infection in the field vole (Microtus agrestis): an ecological model for studies on transmission dynamics. Parasitol Res 114:1703–1709. https://doi.org/10.1007/s00436-015-4355-9
Woolsey ID, Jensen PM, Deplazes P, Kapel CMO (2016) Peroral Echinococcus multilocularis egg inoculation in Myodes glareolus, Mesocricetus auratus and Mus musculus (CD-1 IGS and C57BL/6j). Int J Parasitol Parasites Wildl 5:158–163. https://doi.org/10.1016/j.ijppaw.2016.05.004
Acknowledgements
Danish hunters and the Danish Nature Agency are thanked for supplying carnivores for the surveillance study. Cynthia D Juel, Boi-Tien T Pham, Leif B Eiersted and Aleksandra Tofteby are acknowledged for skilled technical assistance. The Institute of Parasitology, Zurich University (Prof. Deplazes) and The Danish Serum Institut (Dr. Steensvold) are thanked for assistance with the analysis of cysts isolated from rodents. The study was financed by the Danish Veterinary and Food Administration, The Danish Environmental Protection Agency (Grant nr. 410239) and The Technical University of Denmark.
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Petersen, H.H., Al-Sabi, M.N.S., Enemark, H.L. et al. Echinococcus multilocularis in Denmark 2012–2015: high local prevalence in red foxes. Parasitol Res 117, 2577–2584 (2018). https://doi.org/10.1007/s00436-018-5947-y
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DOI: https://doi.org/10.1007/s00436-018-5947-y