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Larval development of Angiostrongylus chabaudi, the causative agent of feline angiostrongylosis, in the snail Cornu aspersum

Published online by Cambridge University Press:  14 August 2017

V. COLELLA Open the ORCID record for V. COLELLA [Opens in a new window] ,
M. A. CAVALERA ,
G. DEAK ,
V. D. TARALLO ,
C. M. GHERMAN ,
A. D. MIHALCA  and
D. OTRANTO
V. COLELLA
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Str. prov. per Casamassima km 3, 70010 Valenzano (Bari), Italy
M. A. CAVALERA
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Str. prov. per Casamassima km 3, 70010 Valenzano (Bari), Italy
G. DEAK
Affiliation:
Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Calea Mănăștur 3-5, 400372 Cluj-Napoca, Romania
V. D. TARALLO
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Str. prov. per Casamassima km 3, 70010 Valenzano (Bari), Italy
C. M. GHERMAN
Affiliation:
Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Calea Mănăștur 3-5, 400372 Cluj-Napoca, Romania
A. D. MIHALCA
Affiliation:
Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine of Cluj-Napoca, Calea Mănăștur 3-5, 400372 Cluj-Napoca, Romania
D. OTRANTO*
Affiliation:
Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Str. prov. per Casamassima km 3, 70010 Valenzano (Bari), Italy
*
*Corresponding author: Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Str. prov. per Casamassima km 3, 70010 Valenzano (Bari), Italy. E-mail: domenico.otranto@uniba.it
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Summary

Nematodes of the Angiostrongylidae family, such as Angiostrongylus vasorum and Angiostrongylus cantonensis, may cause potentially life-threatening diseases in several mammal species. Alongside these well-known species, Angiostrongylus chabaudi has been recently found affecting the cardiopulmonary system of domestic and wild cats from Italy, Germany, Greece, Romania and Bulgaria. Nonetheless, significant gaps in the understanding of A. chabaudi epidemiology include the lack of information of species acting as intermediate host and of the morphological description of larval stages. Cornu aspersum (n = 30) land snails were infected with 100 first-stage larvae of A. chabaudi collected from a naturally infected wildcat in Romania. Larvae at different developmental stages were found in 29 out of 30 (96·7%) infected snails and a total of 282 (mean 9·8 ± 3·02 larvae per each specimen) were collected from the gastropods. Here we demonstrate that A. chabaudi develops in snails and report C. aspersum as potential intermediate host for this parasitic nematode. Findings of this study are central to understand the ecological features of feline angiostrongylosis and its epidemiology within paratenic and intermediate hosts.

Keywords

felinecardiopulmonary nematodelungwormsintermediate hostsnailsCornu aspersum
Type
Research Article
Information
Parasitology , Volume 144 , Issue 14 , December 2017 , pp. 1922 - 1930
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Alfaro-Alarcón, A., Veneziano, V., Galiero, G., Cerrone, A., Gutierrez, N., Chinchilla, A., Annoscia, G., Colella, V., Dantas-Torres, F., Otranto, D. and Santoro, M. (2015). First report of a naturally patent infection of Angiostrongylus costaricensis in a dog. Veterinary Parasitology 212, 431–434.Google Scholar
Alić, A., Traversa, D., Duscher, G. G., Kadrić, M., Di Cesare, A. and Hodžić, A. (2015). Troglostrongylus brevior in an Eurasian lynx (Lynx lynx) from Bosnia and Herzegovina. Parasites & Vectors 8, 653.Google Scholar
Anderson, R. C. (2000). The superfamily Metastrongyloidea. In Nematode Parasites of Vertebrates. Their Development and Transmission (ed. CABI Publishing), pp. 163–164. CAB International, Wallingford, UK.Google Scholar
Ash, L. R. (1970). Diagnostic morphology of the third-stage larvae of Angiostrongylus cantonensis, Angiostrongylus vasorum, Aelurostrongylus abstrusus, and Anafilaroides rostratus (Nematoda: Metastrongyloidea). Journal of Parasitology 56, 249–253.Google Scholar
Biocca, E. (1957). Angiostrongylus chabaudi n. sp. parassita del cuore e dei vasi polmonari del gatto selvatico (Felis silvestris). Reale Accademia Nazionale Lincei 22, 526–532.Google Scholar
Brianti, E., Gaglio, G., Giannetto, S., Annoscia, G., Latrofa, M. S., Dantas-Torres, F., Traversa, D. and Otranto, D. (2012). Troglostrongylus brevior and Troglostrongylus subcrenatus (Strongylida: Crenosomatidae) as agents of broncho-pulmonary infestation in domestic cats. Parasites & Vectors 5, 178.Google Scholar
Brianti, E., Giannetto, S., Dantas-Torres, F. and Otranto, D. (2014). Lungworms of the genus Troglostrongylus (Strongylida: Crenosomatidae): neglected parasites for domestic cats. Veterinary Parasitology 202, 104–112.Google Scholar
Burns, R. E., Bicknese, E. J., Qvarnstrom, Y., DeLeon-Carnes, M., Drew, C. P., Gardiner, C. H. and Rideout, B. A. (2014). Cerebral Angiostrongylus cantonensis infection in a captive African pygmy falcon (Polihierax semitorquatus) in southern California. Journal of Veterinary Diagnostic Investigation 26, 695–698.Google Scholar
Colella, V., Mutafchiev, Y., Cavalera, M. A., Giannelli, A., Lia, R. P., Dantas-Torres, F. and Otranto, D. (2016). Development of Crenosoma vulpis in the common garden snail Cornu aspersum: implications for epidemiological studies. Parasites & Vectors 9, 208.Google Scholar
Deak, G., Gherman, C. M., Ionică, A. M., Daskalaki, A. A., Matei, I. A., D'Amico, G., Domşa, C., Pantchev, N., Mihalca, A. D. and Cozma, V. (2017). Use of a commercial serologic test for Angiostrongylus vasorum for the detection of A. chabaudi in wildcats and A. daskalovi in badgers. Veterinary Parasitology 233, 107–110.Google Scholar
Diakou, A., Di Cesare, A., Barros, L. A., Morelli, S., Halos, L., Beugnet, F. and Traversa, D. (2015). Occurrence of Aelurostrongylus abstrusus and Troglostrongylus brevior in domestic cats in Greece. Parasites & Vectors 8, 590.Google Scholar
Diakou, A., Psalla, D., Migli, D., Di Cesare, A., Youlatos, D., Marcer, F. and Traversa, D. (2016). First evidence of the European wildcat (Felis silvestris silvestris) as definitive host of Angiostrongylus chabaudi . Parasitology Research 115, 1235–1244.Google Scholar
Duffy, M. S., Miller, C. L., Kinsella, J. M. and de Lahunta, A. (2004). Parastrongylus cantonensis in a nonhuman primate. Florida. Emerging Infectious Diseases 10, 2207–2210.Google Scholar
Elsheikha, H. M., Holmes, S. A., Wright, I., Morgan, E. R. and Lacher, D. W. (2014). Recent advances in the epidemiology, clinical and diagnostic features, and control of canine cardio-pulmonary angiostrongylosis. Veterinary Research 45, 92.Google Scholar
Falsone, L., Brianti, E., Gaglio, G., Napoli, E., Anile, S., Mallia, E., Giannelli, A., Poglayen, G., Giannetto, S. and Otranto, D. (2014). The European wildcats (Felis silvestris silvestris) as reservoir hosts of Troglostrongylus brevior (Strongylida: Crenosomatidae) lungworms. Veterinary Parasitology 205, 193–198.Google Scholar
Gasser, R. B., Chilton, N. B., Hoste, H. and Beveridge, I. (1993). Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 2525–2526.CrossRefGoogle ScholarPubMed
Gerichter, C. B. (1949). Studies on the nematodes parasitic in the lungs of Felidae in Palestine. Parasitology 39, 251–262.Google Scholar
Gherman, C. M., Ionică, A. M., D'Amico, G., Otranto, D. and Mihalca, A. D. (2016). Angiostrongylus chabaudi (Biocca, 1957) in wildcat (Felis silvestris silvestris, S) from Romania. Parasitology Research 115, 2511–2517.Google Scholar
Giannelli, A., Ramos, R. A., Annoscia, G., Di Cesare, A., Colella, V., Brianti, E., Dantas-Torres, F., Mutafchiev, Y. and Otranto, D. (2014). Development of the feline lungworms Aelurostrongylus abstrusus and Troglostrongylus brevior in Helix aspersa snails. Parasitology 141, 563–569.Google Scholar
Giannelli, A., Kirkova, Z., Abramo, F., Latrofa, M. S., Campbell, B., Zizzo, N., Cantacessi, C., Dantas-Torres, F. and Otranto, D. (2016). Angiostrongylus chabaudi in felids: new findings and a review of the literature. Veterinary Parasitology 228, 188–192.Google Scholar
Giannelli, A., Capelli, G., Hinney, B., Joachim, A., Losson, B., Kirkova, Z., Martellet, M. R., Papadopoulos, E., Farkas, R., Brianti, E., Tamponi, C., Varcasia, A., Alho, A. M., Madeira de Carvalho, L., Cardoso, L., Maia, C., Mircean, V., Mihalca, A. D., Mirò, G., Schnyder, M., Cantacessi, C., Colella, V., Cavalera, M. A., Latrofa, M. S., Annoscia, G., Halos, L., Knaus, M., Beugnet, F. and Otranto, D. (2017). Epidemiology, diagnosis and treatment of lungworm and gastrointestinal parasitic infections in cats: an European perspective. International Journal for Parasitology, pii: S0020-7519(17)30101-7. doi: 10.1016/j.ijpara.2017.02.003.Google Scholar
Grewal, P. S., Grewal, S. K., Tan, L. and Adams, B. J. (2003). Parasitism of molluscs by nematodes: types of associations and evolutionary trends. Journal of Nematology 35, 146–156.Google Scholar
Grøndahl, C., Monrad, J., Dietz, H. H., Jensen, H. E., Johansen, M. V. and Kapel, C. (2005). Angiostrongylosis in red panda (Ailurus fulgens fulgens). Proceedings of International Symposium of Disease in Zoo and Wild animals 42, 117–118.Google Scholar
Guiller, A., Martin, M. C., Hiraux, C. and Madec, L. (2012). Tracing the invasion of the Mediterranean land snail Cornu aspersum aspersum becoming an agricultural and garden pest in areas recently introduced. PLoS ONE 7, e49674.Google Scholar
Jefferies, R., Vrhovec, M. G., Wallner, N. and Catalan, D. R. (2010). Aelurostrongylus abstrusus and Troglostrongylus sp. (Nematoda: Metastrongyloidea) infections in cats inhabiting Ibiza, Spain. Veterinary Parasitology 173, 344–348.Google Scholar
Kim, J. R., Hayes, K. A., Yeung, N. W. and Cowie, R. H. (2014). Diverse gastropod hosts of Angiostrongylus cantonensis, the rat lungworm, globally and with a focus on the Hawaiian Islands. PLoS ONE 9, e94969.CrossRefGoogle ScholarPubMed
Lange, M. K., Penagos-Tabares, F., Muñoz-Caro, T., Gärtner, U., Mejer, H., Schaper, R., Hermosilla, C. and Taubert, A. (2017). Gastropod-derived haemocyte extracellular traps entrap metastrongyloid larval stages of Angiostrongylus vasorum, Aelurostrongylus abstrusus and Troglostrongylus brevior . Parasites & Vectors 10, 50.Google Scholar
Lunn, J. A., Lee, R., Smaller, J., Mackay, B. M., King, T., Hunt, G. B., Martin, P., Krockenberger, M. B., Spielman, D. and Malik, R. (2012). Twenty two cases of canine neural angiostrongylosis in eastern Australia (2002–2005) and a review of the literature. Parasites & Vectors 5, 70–88.Google Scholar
Madsen, A. B., Dietz, H. H., Henriksen, P. and Clausen, B. (1999). Survey of Danish free living Otters Lutra lutra – a consecutive collection and necroscopy of dead bodies. IUCN Otter Specialist Group Bulletin 16, 65–76.Google Scholar
Morgan, E. R. and Shaw, S. E. (2010). Angiostrongylus vasorum infection in dogs: continuing spread and developments in diagnosis and treatment. Journal of Small Animal Practice 51, 616–621.Google Scholar
Morgan, E. R., Jefferies, R., Krajewski, M., Ward, P. and Shaw, S. E. (2009). Canine pulmonary angiostrongylosis: the influence of climate on parasite distribution. Parasitology International 58, 406–410.Google Scholar
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, 24–37.Google Scholar
Patterson-Kane, J. C., Gibbons, L. M., Jefferies, R., Morgan, E. R., Wenzlow, N. and Redrobe, S. P. (2009). Pneumonia from Angiostrongylus vasorum infection in a red panda (Ailurus fulgens fulgens). Journal of Veterinary Diagnostic Investigation 21, 270–273.Google Scholar
Romero-Alegría, A., Belhassen-García, M., Velasco-Tirado, V., Garcia-Mingo, A., Alvela-Suárez, L., Pardo-Lledias, J. and Sanchez, M. C. (2014). Angiostrongylus costaricensis: systematic review of case reports. Advances in Infectious Diseases 4, 36–41.Google Scholar
Rosen, L., Ash, L. R. and Wallace, G. D. (1970). Life history of the canine lungworm Angiostrongylus vasorum . American Journal of Veterinary Research 31, 131–141.Google ScholarPubMed
Spratt, D. M. (2015). Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: A review. International Journal for Parasitology: Parasites and Wildlife 4, 178–189.Google Scholar
Steeb, S., Hirzmann, J., Eskens, U., Volmer, K. and Bauer, C. (2014). Lungenwurm-Infektionen bei der europäischen wildkatze. KompaktVET 3, 9.Google Scholar
Torres, J., Miquel, J. and Motjé, M. (2001). Helminth parasites of the Eurasian badger (Meles meles L.) in Spain: a biogeographic approach. Parasitology Research 87, 259–263.Google Scholar
Traversa, D., Lepri, E., Veronesi, F., Paoletti, B., Simonato, G., Diaferia, M. and Di Cesare, A. (2015). Metastrongyloid infection by Aelurostrongylus abstrusus, Troglostrongylus brevior and Angiostrongylus chabaudi in a domestic cat. International Journal for Parasitology 45, 685–690.Google Scholar
Varcasia, A., Tamponi, C., Brianti, E., Cabras, P. A., Boi, R., Pipia, A. P., Giannelli, A., Otranto, D. and Scala, A. (2014). Angiostrongylus chabaudi Biocca, 1957: a new parasite for domestic cats? Parasites & Vectors 7, 588.Google Scholar
Veronesi, F., Traversa, D., Lepri, E., Morganti, G., Vercillo, F., Grelli, D., Cassini, R., Marangi, M., Iorio, R., Ragni, B. and Di Cesare, A. (2016). Occurrence of lungworms in European wildcats (Felis silvestris silvestris) of central Italy. Journal of Wildlife Diseases 52, 270–278.Google Scholar
Wang, Q. P., Wu, Z. D., Wei, J., Owen, R. L. and Lun, Z. R. (2012). Human Angiostrongylus cantonensis: an update. European Journal of Clinical Microbiology & Infectious Diseases 31, 389–395.Google Scholar