Angiostrongylus vasorum (Baillet, 1866) Kamensky 1905 is a parasitic nematode of the Metastrongilidae

family that infects the pulmonary artery and right-heart of many carnivore species. The host infection

occurs by the ingestion of the infecting larvae present in aquatic and terrestrial gastropod mollusks. The

infected vertebrate hosts may develop clinical symptoms ranging from asymptomatic to severe

complications. From 2011 to 2013, seven species of canids were found run over on the Mountain Region

highways in the Santa Catarina State, South Brazil. Fecal samples obtained in necropsy were analyzed by

simple spontaneous flotation method. Only one species of Lycalopex gymnocercus (Fischer, 1814) was

diagnosed as infected with A. vasorum. This is the first report of this nematode in this species. Parasitosis

can be considered a health problem in areas where the parasite is endemic and L. gymnocercus is

considered of conservation interest.

ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

ANGIOSTRONGYLUS VASORUM (BAILLET, 1866) KAMENSKY 1905 IN LYCALOPEX

GYMNOCERCUS (FISCHER, 1814) (PAMPAS FOX) IN BRAZIL

ANGIOSTRONGYLUS VASORUM (BAILLET, 1866) KAMENSKY 1905 IN LYCALOPEX

GYMNOCERCUS (FISCHER, 1814) (PAMPAS FOX) IN BRAZIL

1Laboratory of Parasitology and Parasitic Diseases - Agroveterinary Center of the State of Santa Catarina University (CAV-

UDESC), Lages, Santa Catarina, Brasil; Laboratory of Zoology and Parasitology of the Planalto Catarinense University -

UNIPLAC, Lages, Brasil; Scholars of The Veterinary Medicine Course of the Agroveterinary Center of the State of Santa

Catarina University (CAV-UDESC), Lages, Santa Catarina, Brasil

Corresponding author: Rosiléia Marinho de Quadros. Av. Luis de Camões, 2090, Conta dinheiro, Lages-SC,

Brazil. CEP: 88520-000. Fone: 55 49 32899316.

e-mail: biomedvety@gmail.com

ABSTRACT

Key words: Angiostrongylus vasorum - Canid - Lycalopex - Lung parasites - Parasitosis

Neotropical Helminthology

Volume13,Number1(jan-jun2019)

ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)

Lima-Perú

VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043

Auspiciado por:

Neotropical Helminthology, 2019, 13(1), ene-jun:65-71.

1-2 1 4

Rosiléia Marinho de Quadros ; Anderson Barbosa de Moura ; Ruan Bruno Rodrigues ;

4 1

Kellyn Hass Martins & Alessandra Snak

INTRODUCTION

RESUMEN

Palabras clave: Angiostrongylus vasorum - Cánidos - Lycalopex - Parasitos Pulmonares - Parasitosis

Angiostrongylus vasorum (Baillet, 1866) Kamensky 1905 es un nematodo parásito de la familia

Metastrongilidae que infecta la arteria pulmonar y el corazón derecho de muchas especies de carnívoros.

La infección del huésped se produce por la ingestión de las larvas infectantes presentes en los moluscos

gasterópodos terrestres y acuáticos. Los huéspedes vertebrados infectados pueden desarrollar síntomas

clínicos que van desde asintomáticas hasta complicaciones graves. Entre 2011 y 2013, se encontraron

siete especies de cánidos en las carreteras de la región montañosa en el estado de Santa Catarina, sur de

Brasil. Las muestras fecales obtenidas en la necropsia fueron analizadas por un método simple de

flotación espontánea. Sólo la especie Lycalopex gymnocercus (Fischer, 1814) fue diagnosticada con A.

vasorum. Este es el primer reporte de este nematodo en esta especie. La parasitosis puede considerarse un

problema de salud en áreas donde el parásito es endémico y L. gymnocercus se considera de interés para la

conservación.

Linnaeus 1758 (dog), Canis lupus Linnaeus, 1758

(wolf), C. thous (crab eating fox), Vulpes vulpes

Linnaeus, 1758 (red fox), Vulpes zerda

Zimmerman 1780 (desert fox), Meles meles

Linnaeus, 1758 (European badger) and

experimentally some species of rodents like the

Arvicanthis niloticus Desmarest, 1822 and Nile rat

(Bourque et al., 2005). In feline carnivores

(Morgan et al., 2008) and mustelidae like Lutra

lutra Linnaeus, 1758 (otter) and Mustela putorius

Linnaeus, 1758 (ferret) there was also evidence of

these parasites (Koch & Willesen, 2009). Although

human infection has not been confirmed, some

researchers do not discard the zoonotic potential

(Eckert & Lammler, 1972).

The transmission cycle of the parasite occurs with

the ingestion of the third larval stage (L ) in aquatic

gastropods such as Biomphalaria glabrata Say,

1818 and terrestrial ones like Arion spp. Férussac,

1819, Achatina fulica Férussac,1821, Subulina

octona Bruguière, 1789, Bradybaena similis

Férussac,1821, Laevicaulis salte Férussac,1822,

Prosoples javanicum (Bessa et al., 2000; Koch &

Willesen, 2009; Oliveira et al., 2010; Patel et al.,

2014) and Omalonix matheroni (Potiez &

Michaud, 1838), where experimental observation

found the larval development of A. vasorum to be

faster in this mollusk compared to other observed

intermediate hosts (Mozzer et al., 2011).

It has been demonstrated in dogs that the infection

may occur by the ingestion of infected paratenic

The canid family has 16 genera and 36 species with

large geographical distribution, found from the

tropics to the Arctic. Twenty nine earth bound

species, of the Carnivore order, occur in Brazil

(Reis et al., 2007).

In South America there are seven genera and 11

wild canid species (Ruas et at., 2008). In the State

of Santa Catarina there are reports of only two

species Cerdocyon thous and Lycalopex

gymnocercus (Fischer, 1814) (Cherem et al., 2004;

Cherem et al., 2007).

Cerdocyon thous Linnaeus, 1766 is one of the most

known species, being the first canid described in

brazilian literature (Bisbal & Ojasti, 1980). It's

geographic distribution ranges through Uruguay,

northern Argentina, Bolívia, Venezuela, as well as

Guiana, Suriname and Brazil, being found in

almost all biomes, excepting the low areas of the

Amazon basin (Heleno et al., 2011). On the other

hand, L. gymnocercus prefers environments like

open grasslands, andean tropical forests,

woodland, marsh, swamps, pastures and farm land.

Angiostrongylus vasorum (Baillet, 1866)

Kamensky 1905 is a nematode of the Strogylida

order, Metastrongyloidea superfamily, that infects

the pulmonary artery and right heart of many

carnivore species such as Canis familiaris

Neotropical Helminthology, 2019, 13(1), ene-jun Marinho de Quadros et al.

hosts like toads and small mammals.

Experimentally infected birds may also act as

paratenic hosts (Mozzer & Lima, 2015).

Normally, the infection is mild and along with

respiratory manifestations it may evolve to serious

complications like neurological, cardiac and

gastrointestinal disorders (Morgan & Shaw, 2010).

Primary clinical signs are almost exclusively

related to respiratory dysfunction that go from

cough, exercise intolerance, dispnea and cardiac

insufficiency. Non specific clinical signs, like

vomit, diarrhea, anorexia and death have also been

described (Gredal et al., 2011, Morgan & Shaw,

2010). Cat infection by A. abstrusus (Railliet,

1898) tends to be insidious, even in cases that

evolve to clinical symptoms, fatal infection is

relatively rare in this group (Traversa et al., 2010).

The infections are considered endemic, mainly on

the European continent (France, Denmark, Italy,

Spain Switzerland, England and Ireland), as well as

in countries like Uganda, Turkey, Russia, Brazil,

Colombia and Canada (Bourque et al., 2002). The

nematode has also been described in non endemic

countries like Australia and the USA (Jefferies et

al., 2009).

Between 2011 and 2013, seven species of canid

were found run over on the mountain roads of the

State of Santa Catarina, south Brazil (Fig.1). Three

specimens of C. thous (two males and a female),

and four female L. gymnocercus, one of them alive

and another initially alive died of rangeliosis, a

hemaprotozoa that infects canids. All other animals

were killled from the trauma caused by the

collision. The animals were referred by

government agencies in the environmental area to

the Laboratory of Zoology and Parasitology of the

University Planalto Catarinense (UNIPLAC) for

analysis. Parasitological exams were done, with

the spontaneous flotation method (Hoffman et al.,

1934) and simple flotation with a saturated solution

of sodium chloride at 1,182 density (Willis-

Molay).

Neotropical Helminthology, 2019, 13(1), ene-jun

MATERIAL AND METHODS

Figure 1. Location of canids in the mountain region in Santa Catarina state, Southern Brazil.

Ethic aspects: The authors declare that all the

ethical aspects of the country and international

ones were fulfilled.

RESULTS

In the spontaneous sedimentation method the

presence of larvae of approximately 350µm long

Angiostrongylus vasorum in Lycalopex

with a dorsal terminal spine (400X) were observed,

compatible with first stage larvae (L ) of A.

vasorum (Fig. 2), as described by Patterson et al.

(2009).

Figure 2. fecal samples Larva of the first stage (L ) of Angiostrongylus vasorum in the Lycalopex gymnocercus (Vis. 100X).

Detail: terminal spine (400X).

The larval stage was only diagnosed in a young live

animal captured close to the town of Lages, Santa

Catarina. The animal was also submitted to

laboratory exams, the CBC presented 42%

eosinophils (reference in the species is of 3-12%),

this may be due to parasitic infection.

DISCUSSION

hematological alteration was observed without

eosinophilia (Schnyder et al., 2010). Parasitic

eosinophilia is the result of contact between the

parasite and hosts cells. The more complex the

parasites cycle, with somatic migrations, higher the

eosinophile count, when the parasite is limited to

the digestive tube the eosinophile count tends to be

lower (Chauffaille, 2010).

Mozzer et al. (2011) describes that one of the main

abiotic factor for the development of A. vasorum

larvae in gastropods is the temperature. Low

temperatures (18° to 20° C) delay the larvae

development meanwhile high temperatures

accelerate the process. For Ferdushy & Hasan

(2010), as well as corroborating that low

temperatures are important for the survival

maintenance of larvae, the air relative humidity

seems to have no significant influence in larval

viability.

Low temperatures was observed in the Santa

Catarina mountains in winter, an average of 12.6°C

(EPAGRI, 2013), and this climatic condition may

favor the parasite development as observed in

The event of the parasite in tropical, subtropical

and temperate regions may be due to its ability to

adapt to new hosts (Barçante, 2004; Magi et al.,

2009). A. vasorum has been described in endemic

areas as well as in regions previously described as

free (Cesare et al., 2014; Simin et al., 2014).

E o s i n o p h i l i a , r e g e n e r a t i v e a n e m i a ,

thrombocytopenia, with or without clotting

anomalies, may occur in canids infected with A.

vasorum (Cury et al., 2005, Moermans et al.,

2011). In dogs experimentally infected with A.

vasorum, with high parasite load, only a slight

Neotropical Helminthology, 2019, 13(1), ene-jun Marinho de Quadros et al.

European countries where parasitosis is endemic.

The survival of A. vasorum L is highly influenced

by temperature (Ferdushy & Hasan, 2010) and "In

vitro" the survival of L A. vasorum larvae is higher

at low temperatures, and high temperatures are

associated to larger larvae mortality rates (Dias &

Lima, 2012).

In Brazilian wild canids, A., vasorum was

diagnosed Lycalopex vetulus in the State of Minas

Gerais and C. thous in the States of Rio de Janeiro

and Rio Grande do Sul (Duarte et al., 2007).

Canine angiostrongilosis is an emerging disease

which probably has an expansion due climate

factors, the presence of wild canids in urban areas

(facilitating parasite propagation), as well as to

employment of more precise diagnostic methods

(Capogna et al., 2012).

Also, areas occupied by humans allow the

interactions of wild and domestic animals, which

may favor the infection of domestic dogs. Eleni et

al. (2014), in Italy, defined that the cross infection

between wild and domestic animals are important

for the spreading of this parasite.

The great variety of definite hosts may be

important for the distribution of the parasite in new,

non-endemic areas. The potential of new, non-

described, definite hosts may not be excluded

while the parasite is introduced to new

geographical areas (Koch & Willesen, 2009).

For parasites transmitted by gastropods the

dissemination depends on the geographical

distribution of the intermediate hosts, and these

depend on environmental conditions for their

development. Therefore environmental variability

plays its role on the incidence of parasite infection

(Tomlinson et al., 2006). When the environment is

depleted, carnivores seek to vary their diet and,

since mollusks belong to one of the largest filo of

invertebrate in numbers of species, they may easily

be found in nature, and become an alternative for

animals with food restriction.

Traversa et al. (2010) states that more studies are

necessary to explain the relation of climate

variation and parasite distribution, such as

intermediate hosts, levels of larval development, as

well as the transition patterns, in endemic and non

endemic areas, observing if temperature variation

and other abiotic factors may explain the

dissemination of A. vasorum.

As far as diagnose is concerned the main problem is

that parasitosis symptoms are not specific and may

be confused with other pathologies. The fact that

some infected animals are asymptomatic makes it

even harder to have a definite clinical diagnosis

(Barçante, 2004). Along with this, the main

diagnosis tool for this parasite, the Baermann

technique for larvae detection, is not normally

requested by veterinarians (Cesare et al., 2014).

Clinical diagnosis of angiostrongilosis is difficult.

Animals don't always exhibit clinical signs and in

its general form the infection may be confused with

other pathologies. The parasite infection may be a

problem in areas where the parasite is endemic and

L. gymnocercus considered an interesting species

for conservation.

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Neotropical Helminthology, 2019, 13(1), ene-jun Angiostrongylus vasorum in Lycalopex