Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-22T15:55:18.201Z Has data issue: false hasContentIssue false

Conquering Switzerland: the emergence of Angiostrongylus vasorum in foxes over three decades and its rapid regional increase in prevalence contrast with the stable occurrence of lungworms

Published online by Cambridge University Press:  06 May 2020

Nina Gillis-Germitsch
Affiliation:
Vetsuisse-Faculty, Institute of Parasitology, University of Zurich, Zurich, Switzerland Graduate School for Cellular and Biomedical Sciences, University of Bern, Switzerland
Lucienne Tritten
Affiliation:
Vetsuisse-Faculty, Institute of Parasitology, University of Zurich, Zurich, Switzerland
Daniel Hegglin
Affiliation:
Vetsuisse-Faculty, Institute of Parasitology, University of Zurich, Zurich, Switzerland
Peter Deplazes
Affiliation:
Vetsuisse-Faculty, Institute of Parasitology, University of Zurich, Zurich, Switzerland
Manuela Schnyder*
Affiliation:
Vetsuisse-Faculty, Institute of Parasitology, University of Zurich, Zurich, Switzerland
*
Author for correspondence: Manuela Schnyder, E-mail: [email protected]

Abstract

Angiostrongylus vasorum, Crenosoma vulpis and Capillaria aerophila are the most common lungworms of domestic and wild canids. We investigated the short- and long-term lungworm prevalence changes in the Swiss fox population with a focus on A. vasorum. Between 2012 and 2017, lungs and hearts of 533 foxes from north-eastern Switzerland were necropsied and blood samples tested for circulating A. vasorum antigen. Angiostrongylus vasorum prevalence increased steadily from 21.5% in 2012 to 81.8% in 2017. In contrast, C. aerophila and C. vulpis prevalences fluctuated between 41.8 and 74.7%, and 3.6 and 14.9%, respectively. Based on 3955 blood samples collected between 1986 and 2017 from three geographic areas and during four time periods, antigen seropositivity increased from 2.4 to 62.0%. In north-eastern Switzerland, seropositivity was initially low (1.9 and 1.7% in the first two time periods) but increased in the following two decades to 22.2 and 62.0%, respectively. Our findings depict the spectacular expansion of A. vasorum in the past three decades. Regionally, the prevalence in foxes increased 4-fold within 6 years in some regions. This underpins the important role of foxes as reservoir hosts, likely explaining the increasing number of cases of canine angiostrongylosis in Switzerland. Our findings are representative of central Europe and may help anticipating future developments in areas where A. vasorum is present but (still) infrequent.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Al-Sabi, MN, Halasa, T and Kapel, CM (2014) Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark. Acta Parasitologica 59, 98107.CrossRefGoogle ScholarPubMed
Aziz, NA, Daly, E, Allen, S, Rowson, B, Greig, C, Forman, D and Morgan, ER (2016) Distribution of Angiostrongylus vasorum and its gastropod intermediate hosts along the rural-urban gradient in two cities in the United Kingdom, using real time PCR. Parasites & Vectors 9, 56.CrossRefGoogle ScholarPubMed
Bourque, AC, Conboy, G, Miller, LM and Whitney, H (2008) Pathological findings in dogs naturally infected with Angiostrongylus vasorum in Newfoundland and Labrador, Canada. The Journal of Veterinary Diagnostic Investigation 20, 1120.CrossRefGoogle ScholarPubMed
Breitenmoser, U, Müller, U, Kappeler, A and Zanoni, R (2000) Die Endphase der Tollwut in der Schweiz. Schweizer Archiv für Tierheilkunde 147, 447453.Google Scholar
Bwangamoi, O (1972) Angiostrongylus vasorum and other worms in dogs in Uganda. Veterinary Record 91, 267.CrossRefGoogle ScholarPubMed
Cabanova, V, Miterpakova, M, Druga, M, Hurnikova, Z and Valentova, D (2018) GIS-based environmental analysis of fox and canine lungworm distribution: an epidemiological study of Angiostrongylus vasorum and Crenosoma vulpis in red foxes from Slovakia. Parasitology Research 117, 521530.CrossRefGoogle ScholarPubMed
Chandler, WL (1922) Lungworms of foxes. American Fox and Fur Farmer 1, 21.Google Scholar
Chapman, PS, Boag, AK, Guitian, J and Boswood, A (2004) Angiostrongylus vasorum infection in 23 dogs (1999–2002). The Journal of Small Animal Practice 45, 435440.CrossRefGoogle Scholar
Christenson, RO (1935) Studies on the morphology of the common fox lungworm, Capillaria aërophila (Creplin, 1839). Transactions of the American Microscopical Society 54, 145154.CrossRefGoogle Scholar
Christenson, RO (1938) Life history and epidemiological studies on the fox lungworm, Capillaria aerophila (Creplin, 1839). Livro Jubilar Prof. L. Travassos. Rio de Janeiro: Instituto Oswaldo Cruz, 119186.Google Scholar
Clopper, CJ and Pearson, ES (1934) The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26, 404413.CrossRefGoogle Scholar
Conboy, G (2009) Helminth parasites of the canine and feline respiratory tract. The Veterinary Clinics of North America 39, 11091126, vii.CrossRefGoogle ScholarPubMed
Cuillé, J and Darraspen, E (1930) De la Strongylose cardio-pulmonaire du chien. Revue Générale de Médecine Vétérinaire 466, 625639, 694–710.Google Scholar
Deak, G, Gherman, CM, Ionica, AM, Vezendan, AD, D'Amico, G, Matei, IA, Daskalaki, AA, Marian, I, Damian, A, Cozma, V and Mihalca, AD (2017) Angiostrongylus vasorum in Romania: an extensive survey in red foxes, Vulpes vulpes. Parasites & Vectors 10, 330.CrossRefGoogle ScholarPubMed
Demiaszkiewicz, AW, Pyziel, AM, Kuligowska, I and Lachowicz, J (2014) The first report of Angiostrongylus vasorum (Nematoda; Metastrongyloidea) in Poland, in red foxes (Vulpes vulpes). Acta Parasitologica 59, 758762.CrossRefGoogle Scholar
Deplazes, P, Hegglin, D, Gloor, S and Romig, T (2004) Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends in Parasitology 20, 7784.CrossRefGoogle ScholarPubMed
Deplazes, P, Eckert, J, Mathis, A, von Samson-Himmelstjerna, G and Zahner, H (2016) Parasitology in Veterinary Medicine. Wageningen, The Netherlands: Wageningen Academic Publishers.CrossRefGoogle Scholar
Eleni, C, Grifoni, G, Di Egidio, A, Meoli, R and De Liberato, C (2014) Pathological findings of Angiostrongylus vasorum infection in red foxes (Vulpes vulpes) from Central Italy, with the first report of a disseminated infection in this host species. Parasitology Research 113, 12471250.CrossRefGoogle ScholarPubMed
Ewald, D (1993) Prävalenz von Echinococcus multilocularis bei Rotfüchsen (Vulpes vulpes L.) in der Nord-, Ost-und Südschweiz sowie im Fürstentum Liechtenstein (PhD thesis, Phil. II). University of Zurich, Zurich, Switzerland.CrossRefGoogle Scholar
Fischer, C, Reperant, LA, Weber, JM, Hegglin, D and Deplazes, P (2005) Echinococcus multlocularis infections of rural, residential and urban foxes (Vulpes vulpes) in the canton of Geneva, Switzerland. Parasite 12, 339346.CrossRefGoogle Scholar
Folstad, I and Karter, AJ (1992) Parasites, bright males, and the immunocompetence handicap. The American Naturalist 139, 603622.CrossRefGoogle Scholar
Gillis-Germitsch, N, Kapel, CMO, Thamsborg, SM, Deplazes, P and Schnyder, M (2017) Host-specific serological response to Angiostrongylus vasorum infection in red foxes (Vulpes vulpes): implications for parasite epidemiology. Parasitology 144, 11441153.CrossRefGoogle ScholarPubMed
Glaus, T, Schnyder, M, Dennler, M, Tschuor, F, Wenger, M and Sieber-Ruckstuhl, N (2010) Natural infection with Angiostrongylus vasorum: characterisation of 3 dogs with pulmonary hypertension. Schweizer Archiv für Tierheilkunde 152, 331338.CrossRefGoogle ScholarPubMed
Gloor, S (2002) The rise of urban foxes (Vulpes vulpes) in Switzerland and ecological and parasitological aspects of a fox population in the recently colonised city of Zurich (PhD thesis). University of Zurich, Zurich, Switzerland.Google Scholar
Gonseth, Y, Wohlgemuth, T, Sansonnens, B and Buttler, A (2001) Die Biogeographischen Regionen der Schweiz. Erläuterungen und Einteilungsstandard. Umwelt Materialien. Bern, Switzerland: Bundesamt für Umwelt, Wald und Landschaft, 137.Google Scholar
Guerra, D, Hegglin, D, Bacciarini, L, Schnyder, M and Deplazes, P (2014) Stability of the southern European border of Echinococcus multilocularis In the Alps: evidence that Microtus arvalis is a limiting factor. Parasitology 141, 15931602.CrossRefGoogle Scholar
Guilhon, J and Cens, B (1973) Angiostrongylus vasorum (Baillet, 1866): Étude biologique et morphologique. Annales de Parasitologie 48, 567596.CrossRefGoogle Scholar
Hajnalová, M, Svobodová, V, Schnyder, M, Schaper, R and Svoboda, M (2017) Faecal detection of the lungworms Crenosoma vulpis and Angiostrongylus vasorum and serological detection of A. vasorum in dogs from the Czech Republic. Acta Veterinaria Brno 86, 393398.CrossRefGoogle Scholar
Hegglin, D, Bontadina, F, Contesse, P, Gloor, S and Deplazes, P (2007) Plasticity of predation behaviour as a putative driving force for parasite life-cycle dynamics: the case of urban foxes and Echinococcus multilocularis tapeworm. Functional Ecology 21, 552560.CrossRefGoogle Scholar
Helm, J, Roberts, L, Jefferies, R, Shaw, SE and Morgan, ER (2015) Epidemiological survey of Angiostrongylus vasorum in dogs and slugs around a new endemic focus in Scotland. The Veterinary Record 177, 16.CrossRefGoogle ScholarPubMed
Hermosilla, C, Kleinertz, S, Silva, LM, Hirzmann, J, Huber, D, Kusak, J and Taubert, A (2017) Protozoan and helminth parasite fauna of free-living Croatian wild wolves (Canis lupus) analyzed by scat collection. Veterinary Parasitology 233, 1419.CrossRefGoogle ScholarPubMed
Hofer, S, Gloor, S, Muller, U, Mathis, A, Hegglin, D and Deplazes, P (2000) High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland. Parasitology 120, 135142.CrossRefGoogle ScholarPubMed
Holmes, P and Kelly, J (1973) Capillaria aerophila in the domestic cat in Australia. Australian Veterinary Journal 49, 472473.CrossRefGoogle ScholarPubMed
Houpin, E, McCarthy, G, Ferrand, M, De Waal, T, O'Neill, EJ and Zintl, A (2016) Comparison of three methods for the detection of Angiostrongylus vasorum in the final host. Veterinary Parasitology 220, 5458.CrossRefGoogle ScholarPubMed
Hurnikova, Z, Miterpakova, M and Mandelik, R (2013) First autochthonous case of canine Angiostrongylus vasorum in Slovakia. Parasitology Research 112, 35053508.CrossRefGoogle ScholarPubMed
Jefferies, R, Shaw, SE, Willesen, J, Viney, ME and Morgan, ER (2010) Elucidating the spread of the emerging canid nematode Angiostrongylus vasorum between Palaearctic and Nearctic ecozones. Infection, Genetics and Evolution 10, 561568.CrossRefGoogle ScholarPubMed
Jeffery, RA, Lankester, MW, McGrath, MJ and Whitney, HG (2004) Angiostrongylus vasorum and Crenosoma vulpis in red foxes (Vulpes vulpes) in Newfoundland, Canada. Canadian Journal of Zoology 82, 6674.CrossRefGoogle Scholar
Jolly, S, Poncelet, L, Lempereur, L, Caron, Y, Bayrou, C, Cassart, D, Grimm, F and Losson, B (2015) First report of a fatal autochthonous canine Angiostrongylus vasorum infection in Belgium. Parasitology International 64, 9799.CrossRefGoogle ScholarPubMed
Kistler, WM, Brown, JD, Allison, AB, Nemeth, NM and Yabsley, MJ (2014) First report of Angiostrongylus vasorum and Hepatozoon from a red fox (Vulpes vulpes) from West Virginia, USA. Veterinary Parasitology 200, 216220.CrossRefGoogle ScholarPubMed
Klein, SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247264.CrossRefGoogle ScholarPubMed
Koch, J and Willesen, JL (2009) Canine pulmonary angiostrongylosis: an update. The Veterinary Journal 179, 348359.CrossRefGoogle ScholarPubMed
Koller, B, Hegglin, D and Schnyder, M (2019) A grid-cell based fecal sampling scheme reveals: land-use and altitude affect prevalence rates of Angiostrongylus vasorum and other parasites of red foxes (Vulpes vulpes). Parasitology Research 118, 22352245.CrossRefGoogle Scholar
Lange, MK, Penagos-Tabares, F, Hirzmann, J, Failing, K, Schaper, R, Van Bourgonie, YR, Backeljau, T, Hermosilla, C and Taubert, A (2018) Prevalence of Angiostrongylus vasorum, Aelurostrongylus abstrusus and Crenosoma vulpis larvae in native slug populations in Germany. Veterinary Parasitology 254, 120130.CrossRefGoogle ScholarPubMed
Lurati, L, Deplazes, P, Hegglin, D and Schnyder, M (2015) Seroepidemiological survey and spatial analysis of the occurrence of Angiostrongylus vasorum in Swiss dogs in relation to biogeographic aspects. Veterinary Parasitology 212, 219226.CrossRefGoogle ScholarPubMed
Maksimov, P, Hermosilla, C, Taubert, A, Staubach, C, Sauter-Louis, C, Conraths, FJ, Vrhovec, MG and Pantchev, N (2017) GIS-supported epidemiological analysis on canine Angiostrongylus vasorum and Crenosoma vulpis infections in Germany. Parasites & Vectors 10, 108.CrossRefGoogle ScholarPubMed
Martinez-Rondan, FJ, Ruiz de Ybanez, MR, Lopez-Beceiro, AM, Fidalgo, LE, Berriatua, E, Lahat, L, Sacristan, I, Oleaga, A and Martinez-Carrasco, C (2019) Cardiopulmonary nematode infections in wild canids: Does the key lie on host-prey-parasite evolution? Research in Veterinary Science 126, 5158.CrossRefGoogle ScholarPubMed
Morgan, ER, Tomlinson, A, Hunter, S, Nichols, T, Roberts, E, Fox, MT and Taylor, MA (2008) Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Veterinary Parasitology 154, 4857.CrossRefGoogle Scholar
Morgan, ER, Jefferies, R, Krajewski, M, Ward, P and Shaw, SE (2009) Canine pulmonary angiostrongylosis: the influence of climate on parasite distribution. Parasitology International 58, 406410.CrossRefGoogle ScholarPubMed
Otranto, D and Deplazes, P (2019) Zoonotic nematodes of wild carnivores. International Journal of Parasitology: Parasites and Wildlife 9, 370383.Google ScholarPubMed
Otranto, D, Cantacessi, C, Dantas-Torres, F, Brianti, E, Pfeffer, M, Genchi, C, Guberti, V, Capelli, G and Deplazes, P (2015) The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part II: Helminths and arthropods. Veterinary Parasitology 213, 2437.CrossRefGoogle ScholarPubMed
Philbey, AW and Delgado, D (2013) Detection of Angiostrongylus vasorum in red foxes in Scotland. Veterinary Record 173, 148148.CrossRefGoogle ScholarPubMed
Poli, A, Arispici, M, Mancianti, F and Abramo, F (1991) Pathology of naturally acquired Angiostrongylus vasorum infection in the red fox (Vulpes vulpes). Angewandte Parasitologie 32, 121126.Google Scholar
Poulin, R (1996) Sexual inequalities in helminth infections: a cost of being a male? The American Naturalist 147, 287295.CrossRefGoogle Scholar
Priest, JM, Stewart, DT, Boudreau, M, Power, J and Shutler, D (2018) First report of Angiostrongylus vasorum in coyotes in mainland North America. Veterinary Record 183, 747.CrossRefGoogle ScholarPubMed
Saeed, I, Maddox-Hyttel, C, Monrad, J and Kapel, CM (2006) Helminths of red foxes (Vulpes vulpes) in Denmark. Veterinary Parasitology 139, 168179.CrossRefGoogle ScholarPubMed
Schnyder, M, Fahrion, A, Riond, B, Ossent, P, Webster, P, Kranjc, A, Glaus, T and Deplazes, P (2010) Clinical, laboratory and pathological findings in dogs experimentally infected with Angiostrongylus vasorum. Parasitology Research 107, 14711480.CrossRefGoogle ScholarPubMed
Schnyder, M, Tanner, I, Webster, P, Barutzki, D and Deplazes, P (2011) An ELISA for sensitive and specific detection of circulating antigen of Angiostrongylus vasorum in serum samples of naturally and experimentally infected dogs. Veterinary Parasitology 179, 152158.CrossRefGoogle ScholarPubMed
Schucan, A, Schnyder, M, Tanner, I, Barutzki, D, Traversa, D and Deplazes, P (2012) Detection of specific antibodies in dogs infected with Angiostrongylus vasorum. Veterinary Parasitology 185, 216224.CrossRefGoogle ScholarPubMed
Serres, E (1854) Entozoaires trouvés dans l'oreille droite, le ventricule correspondant et l'artère pulmonaire d'un chien. Journal des Vétérinaires du Midi 7, 70.Google Scholar
Sigrist, NE, Hofer-Inteeworn, N, Jud Schefer, R, Kuemmerle-Fraune, C, Schnyder, M and Kutter, APN (2017) Hyperfibrinolysis and hypofibrinogenemia diagnosed with rotational thromboelastometry in dogs naturally infected with Angiostrongylus vasorum. Journal of Veterinary Internal Medicine 31, 10911099.CrossRefGoogle ScholarPubMed
Simpson, VR (1996) Angiostrongylus vasorum infection in foxes (Vulpes vulpes) in Cornwall. Veterinary Record 139, 443445.CrossRefGoogle Scholar
Sreter, T, Szell, Z, Marucci, G, Pozio, E and Varga, I (2003) Extraintestinal nematode infections of red foxes (Vulpes vulpes) in Hungary. Veterinary Parasitology 115, 329334.CrossRefGoogle Scholar
Staebler, S, Ochs, H, Steffen, F, Naegeli, F, Borel, N, Sieber-Ruckstuhl, N and Deplazes, P (2005) Autochthone Infektionen mit Angiostrongylus vasorum bei Hunden in der Schweiz und Deutschland. Schweizer Archiv für Tierheilkunde 147, 121127.CrossRefGoogle Scholar
Stockdale, PH and Hulland, TJ (1970) The pathogenesis, route of migration, and development of Crenosoma vulpis in the dog. Pathologica Veterinaria 7, 2842.CrossRefGoogle ScholarPubMed
Tanner, F, Hegglin, D, Thoma, R, Brosi, G and Deplazes, P (2006) Echinococcus multilocularis in Graubünden: Verbreitung bei Füchsen und Vorkommen potentieller Zwischenwirte. Schweizer Archiv für Tierheilkunde 148, 501510.CrossRefGoogle Scholar
Taylor, CS, Garcia Gato, R, Learmount, J, Aziz, NA, Montgomery, C, Rose, H, Coulthwaite, CL, McGarry, JW, Forman, DW, Allen, S, Wall, R and Morgan, ER (2015) Increased prevalence and geographic spread of the cardiopulmonary nematode Angiostrongylus vasorum in fox populations in Great Britain. Parasitology 142, 11901195.CrossRefGoogle ScholarPubMed
Tolnai, Z, Szell, Z and Sreter, T (2015) Environmental determinants of the spatial distribution of Angiostrongylus vasorum, Crenosoma vulpis and Eucoleus aerophilus in Hungary. Veterinary Parasitology 207, 355358.CrossRefGoogle ScholarPubMed
Traversa, D, Morelli, S, Cassini, R, Crisi, PE, Russi, I, Grillotti, E, Manzocchi, S, Simonato, G, Beraldo, P, Viglietti, A, De Tommaso, C, Pezzuto, C, Pampurini, F, Schaper, R and Frangipane di Regalbono, A (2019) Occurrence of canine and feline extra-intestinal nematodes in key endemic regions of Italy. Acta Tropica 193, 227235.CrossRefGoogle ScholarPubMed
Webster, P, Monrad, J, Kapel, CMO, Kristensen, AT, Jensen, AL and Thamsborg, SM (2017) The effect of host age and inoculation dose on infection dynamics of Angiostrongylus vasorum in red foxes (Vulpes vulpes). Parasites & Vectors 10, 4.CrossRefGoogle Scholar
Wetzel, R (1940) Zur Biologie des Fuchslungenwurmes Crenosoma vulpis. Archiv für Wissenschaftliche und Praktische Tierheilkunde 75, 445450.Google Scholar
Willingham, AL, Ockens, NW, Kapel, CMO and Monrad, J (1996) A helminthological survey of wild red foxes (Vulpes vulpes) from the metropolitan area of Copenhagen. Journal of Helminthology 70, 259263.CrossRefGoogle ScholarPubMed
Wolff, K, Eckert, J andLeemann, W (1969) Beitrag zur Angiostrongylose des Hundes. In: Congress of the Dtsch. Vet-med Ges., Fachgr. ‘Kleintierkrankheiten’, Zürich.Google Scholar
Woolsey, ID, Webster, P, Thamsborg, S, Schnyder, M, Monrad, J and Kapel, CMO (2017) Repeated inoculations with the lung and heartworm nematode Angiostrongylus vasorum result in increasing larval excretion and worm burden in the red fox (Vulpes vulpes). International Journal of Parasitology: Parasites and Wildlife 6, 139145.Google Scholar
Supplementary material: File

Gillis-Germitsch et al. supplementary material

Gillis-Germitsch et al. supplementary material 1

Download Gillis-Germitsch et al. supplementary material(File)
File 17 KB
Supplementary material: PDF

Gillis-Germitsch et al. supplementary material

Gillis-Germitsch et al. supplementary material 2

Download Gillis-Germitsch et al. supplementary material(PDF)
PDF 216.6 KB