Skip to main content Accessibility help
×
Home

Angiostrongylosis in Cerdocyon thous (crab-eating fox) and Lycalopex gymnocercus (Pampas fox) in Southern Brazil

  • Rafaela A. Caprioli (a1), Caroline P. de Andrade (a1), Fernando F. Argenta (a1), Luiza P. Ehlers (a1), João Fábio Soares (a1), Saulo P. Pavarini (a1), David Driemeier (a1) and Luciana Sonne (a1)...

Abstract

The objective of this study was to identify species of Angiostrongylus spp. infecting wild carnivores in Southern Brazil, as well as to describe gross and histopathological findings associated with the infection. Necropsy was conducted in 16 wild carnivores parasitized by Angiostrongylus spp. Analysed lungs revealed multifocal dark-red areas of consolidation; in one case, multifocal firm white nodules spread in all pulmonary lobes were observed. In one animal, a focally extensive area of malacia associated with haemorrhage was noted in the encephalon. Histologically, multifocal granulomatous pneumonia or bronchopneumonia, associated with eggs and larvae in blood vessels, lung interstitium, alveoli, and sometimes in bronchi and bronchioles was observed. Adult nematodes were seen within blood vessels. The lesion observed in the brain was characterized as a focally extensive area of malacia associated with gitter cells, haemorrhage, thrombosis and a free intralesional larva. Through molecular techniques, seven positive samples of Angiostrongylus cantonensis were obtained, including the brain sample, and a positive sample of Angiostrongylus vasorum-like, all in Cerdocyon thous. The positive sample for A. vasorum showed 97% similarity with sequences deposited in GenBank, suggesting a new species or subspecies of Angiostrongylus sp. Infection of Lycalopex gymnocercus by Angiostrongylus spp. was confirmed by histological evaluation.

Copyright

Corresponding author

Author for correspondence: Rafaela A. Caprioli, E-mail: rafa_caprioli@hotmail.com

Footnotes

Hide All
*

Laboratory of Protozoology and Vector-borne Rickettsiosis, Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil.

Footnotes

References

Hide All
Acha, P and Szyfres, B (2003) Zoonoses and Communicable Diseases Man and Animals, 3rd Edn. Washington, DC: Pan American Health Organization, Scientific and Tech Publications.
Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403410.
Blaxter, ML, De Ley, P, Garey, JR, Liu, LX, Scheldeman, P, Vierstraete, A, Vanfleteren, JR, Mackey, LY, Dorris, M, Frisse, LM, Vida, JT and Thomas, WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392, 7175.
Bourque, A, Whitney, H and Conboy, G (2005) Angiostrongylus vasorum infection in coyote (Canis latrans) from Newfoundlandand Labrador, Canada. Journal of Wildlife Diseases 41, 816819.
Costa, LRR, McCluret, JJ, Snideirii, G and Stewart, TB (2000) Verminous meningoencephalomyelitis by Angiostrongy zus (=Parastrongylus) cantonensis in an American miniature horse. Equine Veterinary Education 12, 26.
Denk, D, Matiasek, K, Just, FT, Hermanns, W, Baiker, K, Herbach, N, Steinberg, T and Fischer, A (2009) Disseminated angiostrongylosis with fatal cerebral haemorrhages in two dogs in Germany: a clinical case study. Veterinary Parasitology 160, 100108.
Duarte, FH, Vieira, FM, Louzada, GL, Bessa, ECA and Souzalima, S (2007) Occurrence Angiostrongylus vasorum (Baillet, 1866) (Nematoda, Angiostrongylidae) in Cerdocyon thous Linnaeus, 1766 (Carnivora, Canidae) in Minas Gerais State Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 59, 10861088.
Eamsobhana, P and Yong, HS (2009) Immunological diagnosis of human angiostrongyliasis due to Angiostrongylus cantonensis (Nematoda: Angiostrongylidae). International Journal of Infectious Diseases 13, 425431.
Eleni, C, De Liberato, C, Azam, D, Morgan, ER and Traversa, D (2014) Angiostrongylus vasorum in wolves in Italy. International Journal for Parasitology: Parasites and Wildlife 3, 1214.
Ferreira-Júnior, JA, Blume, GR, Sousa, SKH, Carvalho, CM and Gardiner, C (2017) Anatomopathological aspects of parasitism by nematodes of the superfamily Metastrongyloidea in wild crab-eating fox (Cerdocyon thous) in Midwestern Brazil. Ciência Rural 47, 14.
Foronda, P, Lopez-Gonzalez, M, Miquel, J, Torres, J, Segovia, M, Abreu-Acosta, N, Casanova, JC, Valladares, B, Mas-Coma, S, Bargues, MD and Feliu, C (2010) Finding of Parastrongylus cantonensis (Chen, 1935) in Rattus rattus in Tenerife, Canary Islands (Spain). Acta Tropica 114, 123127.
Garosi, LS, Platt, SR, McConnell, JF, Wray, JD and Smith, KC (2005) Intracranial haemorrhage associated with Angiostrongylus vasorum infection in three dogs. Journal of Small Animal Practice 46, 9399.
Graeff-Teixeira, C, Silva, AC and Yoshimura, K (2009) Update on eosinophilic meningoencephalitis and its clinical relevance. Clinical Microbiology Reviews 22, 322348.
Jefferies, R, Shaw, SE, Viney, ME and Morgan, ER (2009) Angiostrongylus vasorum from South America and Europe represent distinct lineages. Parasitology 136, 107115.
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.
Kamenov, Y, Radev, V and Slateva, N (1999) On diagnosis and clinic of angiostrongylosis of cats. Experimental and Molecular Pathology 2, 5154.
Kim, DY, Stewart, TB, Bauer, RW and Mitchell, M (2002) Parastrongylus (=Angiostrongylus) cantonensis now Endemic in Louisiana Wildlife. Journal of Parasitology 88, 10241026.
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.
Koch, J and Willesen, JL (2009) Canine pulmonary angiostrongylosis: an update. The Veterinary Journal 179, 348359.
Li, DN, He, A, Wang, Y, Liang, Y, Li, ZY, Men, JX and Zhan, XM (2001) Three lethal cases of Angiostrongylus cantonensis infected children. Chung-Kuo Chi Sheng Chung Hsueh Yu Chi Sheng Chung Ping Tsa Chih. Chinese Journal Parasitology and Parasitic Diseases 19, 310311.
Lima, WS, Guimarães, MP and Lemos, IS (1994) Occurrence of Angiostrongylus vasorum in the lungs of the Brazilian fox Dusicyon vetulus. Journal of Helminthology 68, 87.
Lunn, JA, Lee, R, Smaller, J, MacKay, BM, King, T and Hunt, GB (2012) Twenty-two cases of canine neural angiostronglyosis in eastern Australia (2002–2005) and a review of the literature. Parasites and Vectors 5, 70.
Ma, G, Dennis, M, Rose, K, Spratt, D and Spielman, D (2013) Tawny frogmouths and brushtail possums as sentinels for Angiostrongylus cantonensis, the rat lungworm. Veterinary Parasitology 192, 158165.
Mason, KV, Prescott, CW, Kelly, WR and Waddell, AL (1976) Granulomatous encephalomyelitis of puppies due to Angiostrongylus cantonensis. Australian Veterinary Journal 52, 295.
McKenzie, RA, Green, PE and Wood, AD (1978) Angiostrongylus cantonensis infection of the brain of a captive Bennett's wallaby (Macropus rufogriseus). Australian Veterinary Journal 54, 8688.
Miething, F, Hering, S, Hanschke, B and Dressler, J (2006) Effect of fixation to the degradation of nuclear and mitochondrial DNA in different tissues. Journal of Histochemistry & Cytochemistry 39, 351354.
Morassutti, AL, Thiengo, SC, Fernandez, M, Sawanyawisuth, K and Graeff-Teixeira, C (2014) Eosinophilic meningitis caused by Angiostrongylus cantonensis: an emergent disease in Brazil. Memórias do Instituto Oswaldo Cruz 109, 399407.
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.
Poli, A, Arispici, M, Marroncini, A, Mancianti, F and de Monte, D (1984) Angiostrongylus vasorum (Baillet, 1886) in red foxes (Vulpes vulpes L.) in Italy. Journal of Wildlife Diseases 20, 345346.
Prociv, P, Spratt, DM and Carlisle, MS (2000) Neuro-angiostrongyliasis: unresolved issues. International Journal for Parasitology 30, 12951303.
Qvarnstrom, Y, Silva, ACA, Teem, JL, Hollingsworth, R, Bishop, H, Graeff-Teixeira, C and Silva, AJ (2010) Improved molecular detection of Angiostrongylus cantonensis in mollusks and other environmental samples with a species-specific internal transcribed spacer 1-based TaqMan assay. Applied and Environmental Microbiology 76, 52875289.
Reddacliff, LA, Bellamy, TA and Hartley, WJ (1999) Angiostrongylus cantonensis infection in grey-headed fruitbats (Pteropus poliocephalus). Australian Veterinary Journal 77, 466468.
Robles, MR, Kinsella, JM, Galliari, C and Navone, GT (2016) New host, geographic records, and histopathologic studies of Angiostrongylus spp (Nematoda: Angiostrongylidae) in rodents from Argentina with updated summary of records from rodent hosts and host specificity assessment. Memórias do Instituto Oswaldo Cruz 111, 181191.
Santoro, M, D'Alessio, N, Di Prisco, F, Neola, B, Restucci, B, Pagano, TB and Veneziano, V (2015) Angiostrongylus vasorum infection in red foxes (Vulpes vulpes) in southern Italy. Acta Parasitologica 60, 356359.
Segovia, JM, Torres, J, Miquel, J, Llaneza, L and Felie, C (2001) Helminths in the wolf, Canis lupus, from north-western Spain. Journal of Helminthology 75, 183192.
Simpson, VR, Tomlinson, AJ, Stevenson, K, McLuckie, JA, Benavides, J and Dagleish, MP (2016) A post-mortem study of respiratory disease in small mustelids in south-west England. BMC Veterinary Research 12, 72.
Staden, R, Judge, DP and Bonfield, JK (2003) Managing sequencing projects in the GAP4 environment. In Krawetz, SA and Womble, DD (eds), Introduction to Bioinformatics. Totawa, NJ: Human Press, pp. 327344.
Tamura, K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Molecular Biology and Evolution 9, 678687.
Thiengo, SC, Simões, RO, Fernandez, MA and Júnior, AM (2013) Angiostrongylus cantonensis and rat lungworm disease in Brazil. Hawai'i Journal of Medicine & Public Health 72, 1822.
Thompson, JD, Higgins, DG, Gibson, TJ and Clustal, W (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.
Torres, J, Miquel, J and Motjé, M (2004) Helminth parasites of the Eurasian badger (Meles meles L.) in Spain: a biogeographic approach. Parasitology Research 87, 259263.
Travassos, L (1927) Novos nematódeos. Boletim biológico 6, 5261.
Traversa, D, Torbidone, A, Malatesta, D and Guglielmini, C (2008) Occurrence of fatal canine Angiostrongylus vasorum infection in Italy. Veterinary Parasitology 152, 162166.
Vieira, FM, Muniz-Pereira, LC, Souzalima, S, Rocha, BM and Luque, JL (2017) Parasitic nematodes of three species of wild carnivore mammals from Atlantic forest in the state of Minas Gerais, Brazil. Revista Mexicana de Biodiversidad 88, 801806.
Wang, X, Tedford, RH, Van Valkenburgh, B and Wayne, RK (2004) Ancestry: evolutionary history, molecular systematics, and evolutionary ecology of Canidae. In MacDonald, DW and Sillero-Zubiri, C (eds), The Biology and Conservation of Wild Canids. Oxford, UK: Oxford University Press, pp. 3954.
Wessmann, A, Lu, D, Lamb, CR, Smyth, B, Mantis, P, Chandler, K, Boag, A, Cherubini, GB and Cappello, R (2006) Brain and spinal cord haemorrhages associated with Angiostrongylus vasorum infection in four dogs. Veterinary Record 158, 858863.

Keywords

Angiostrongylosis in Cerdocyon thous (crab-eating fox) and Lycalopex gymnocercus (Pampas fox) in Southern Brazil

  • Rafaela A. Caprioli (a1), Caroline P. de Andrade (a1), Fernando F. Argenta (a1), Luiza P. Ehlers (a1), João Fábio Soares (a1), Saulo P. Pavarini (a1), David Driemeier (a1) and Luciana Sonne (a1)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed