First record of Lagochilascaris minor (Nematoda: Ascarididae) in Leopardus geoffroyi (Carnivora: Felidae) in Brazil

Primeiro registro de Lagochilascaris minor (Nematoda: Ascarididae) em Leopardus geoffroyi (Carnivora: Felidae) no Brasil

Maira Aparecida Christello Trindade Márcia Raquel Pegoraro de Macedo César Jaeger Drehmer Gertrud Muller About the authors

Abstract

Lagochilascariasis is a parasitic disease caused by nematodes of the genus Lagochilascaris. These parasites occur in the neotropical region and their definitive hosts are wild animals, domestic dogs and felids and, accidentally, humans. Here, infection by Lagochilascaris minor is recorded for the first time in a wild felid, in Brazil.

Keywords:
Lagochilascariasis; “Geoffroy’s cat”; natural infection; wild felid

Resumo

A lagochilascaríase é uma doença parasitária causada por nematoides do gênero Lagochilascaris. Com distribuição neotropical, este parasito tem como hospedeiros definitivos animais silvestres, canídeos e felídeos domésticos e, acidentalmente, seres humanos. Registra-se a primeira ocorrência de Lagochilascaris minor em um felídeo silvestre no Brasil.

Palavras-chave:
Lagochilascaríase; “Gato-do-mato”; infecção natural; felino silvestre

Introduction

Lagochilascariasis is a parasitic disease caused by nematodes of the genus Lagochilascaris Leiper, 1909 (PALHETA-NETO et al., 2002Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol 2002; 68(1): 101-105. http://dx.doi.org/10.1590/S0034-72992002000100018.
http://dx.doi.org/10.1590/S0034-72992002...
). Adult worms infect the oesophagus, pharynx, trachea, related tissues (rhino-oropharynx), and cervical lymphonodes of the definitive hosts (wild animals, dogs and domestic cats, and humans) (CAMPOS et al., 1992Campos DMB, Freire Filha LG, Vieira MA, Paço JM, Maia MA. Experimental life cycle of Lagochilascaris minor Leiper, 1909. Rev Inst Med Trop São Paulo 1992; 34(4): 277-287. http://dx.doi.org/10.1590/S0036-46651992000400003. PMid:1342084.
http://dx.doi.org/10.1590/S0036-46651992...
, 2017Campos DMB, Barbosa AP, Oliveira JA, Tavares GG, Cravo PVL, Ostermayer AL. Human lagochilascariasis – A rare helminthic disease. PLoS Negl Trop Dis 2017; 11(6): e0005510. http://dx.doi.org/10.1371/journal.pntd.0005510. PMid:28640884.
http://dx.doi.org/10.1371/journal.pntd.0...
).

There are five currently valid species: Lagochilascaris minor Leiper, 1909; Lagochilascaris major Leiper, 1910; Lagochilascaris turgida (Stossich, 1902) Travassos, 1924; Lagochilascaris buckleyi Sprent, 1971; and Lagochilascaris sprenti Bowman, Smith and Little, 1983. In South America, L. major and L. minor have been described as parasitizing felids. However, only L. minor has been correlated with human pathological conditions, and this species is therefore considered to have greatest importance of public health (PALHETA-NETO et al., 2002Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol 2002; 68(1): 101-105. http://dx.doi.org/10.1590/S0034-72992002000100018.
http://dx.doi.org/10.1590/S0034-72992002...
).

Leopardus geoffroyi (d’Orbigny & Gervais, 1844), popularly known as “Geoffroy's cat”, is a small neotropical felid that is found across an area extending from south-eastern Bolivia to southern Argentina and Chile (PEREIRA et al., 2015Pereira J, Lucherini M, Trigo T. The IUCN Red List of Treatened Species. Leopardus geoffroyi [online]. 2015 [cited 2019 June 10]. Available from: https://www.iucnredlist.org/species/15310/50657011
https://www.iucnredlist.org/species/1531...
). In Brazil, the species occurs only in the state of Rio Grande do Sul (OLIVEIRA & CASSARO, 2005Oliveira TG, Cassaro K. Guia de campo dos Felinos do Brasil. São Paulo: Instituto Pró-Carnivoros, Sociedade de Zoológicos do Brasil, Fundação Parque Zoológico de São Paulo e Pró-vida Brasil; 2005.). These animals have nocturnal habits and solitary behavior, and their diet is made up of small mammals and other vertebrates (BISCEGLIA et al., 2008Bisceglia SBC, Pereira JA, Teta P, Quintana RD. Food habits of Geoffroy’s cat (Leopardus geoffroyi) in the central Monte desert of Argentina. J Arid Environ 2008; 72(6): 1120-1126. http://dx.doi.org/10.1016/j.jaridenv.2007.11.003.
http://dx.doi.org/10.1016/j.jaridenv.200...
).

The parasitic fauna of this species has been little studied, as is the case with other neotropical carnivores. It is known that the helminth fauna of Geoffroy's cat is composed of 19 taxa: Nematoda (9), Cestoda (8) and Acanthocephala (2), for which records exist mainly in Brazil, Argentina and Paraguay (Table 1). This paper reports the first occurrence of parasitism by L. minor in L. geoffroyi in Brazil.

Table 1
Helminth fauna of Leopardus geoffroyi in different regions of South America.

Materials and Methods

In November 2012, a male specimen of L. geoffroyi was found dead in the municipality of Pelotas (31 ° 46'19 “S; 52 ° 20'34” W), in the south of the state of Rio Grande do Sul, Brazil. It was collected and taken to the Laboratório de Zoologia de Vertebrados of the Universidade Federal de Pelotas (UFPel) for osteological study. The gastrointestinal, respiratory and urinary tracts were donated to the Laboratório de Parasitologia de Animais Silvestres (LAPASIL) of UFPel for parasitological study. We received permission to conduct the study from the Coordinating Council for Teaching, Research and Extension from Universidade de Pelotas, reference COCEPE 234 7861-06/07/2017.

The organs were sectioned, opened and washed with running water in a sieve (150μm mesh). The mucosa and the resulting lavage content were examined under a stereomicroscope. The nematodes were quantified, washed in physiological solution, fixed in cold A.F.A and stored in 70% ethanol. Subsequently, they were clarified with Amann's lactophenol, mounted on semi-permanent slides and viewed under a microscope to perfom morphometric and morphological identifications, in accordance with the description of Sprent (1971a)Sprent JFA. Speciation and development in the genus Lagochilascaris. Parasitology 1971a; 62(1): 71-112. http://dx.doi.org/10.1017/S0031182000071316. PMid:5550315.
http://dx.doi.org/10.1017/S0031182000071...
, Costa et al. (1986)Costa HMA, Silva AVM, Costa PR, Assis SB. Lagochilascaris minor Leiper, 1909, (Nematoda-Ascaridae) de origem humana. Rev Inst Med Trop São Paulo 1986; 28(2): 126-130. http://dx.doi.org/10.1590/S0036-46651986000200009. PMid:3797950.
http://dx.doi.org/10.1590/S0036-46651986...
and Bowman et al. (2002)Bowman DD, Hendrix CM, Lindsay DS, Barr SC. Feline clinical parasitology. Ames: ISU Press; 2002. http://dx.doi.org/10.1002/9780470376805.
http://dx.doi.org/10.1002/9780470376805...
. The specimens were deposited in the Helminth Collection of the Laboratório de Parasitologia de Animais Silvestres, Instituto de Biologia, Universidade Federal de Pelotas (CHLAPASIL/UFPel) (No. 825).

Results and Discussion

Three female and two male nematodes, all in the adult form, were found in the trachea and esophagus.

The following morphological characteristics were used in identifying L. minor: presence of three lips that were wider than long with well-developed cuticular covering; presence of a post-labial deep groove (Figure 1a); posterior margin of the groove forming three triangular interlabial projections; undeveloped lateral alae present along almost the entire length; male with two alate spicules that were smaller than the ejaculatory duct (Figure 1b), equivalent to 33% of the length of the duct (Table 2); and females with vulvar opening located near the middle of the body (Table 2); Eggs were observed in the uterus and presented no more than 25 sculptured pits in their surface (Figure 1c) as described by Volcán et al. (1992)Volcán GS, Medrano CE, Payares G. Experimental heteroxenous cycle of Lagochilascaris minor Leiper, 1909 (Nematoda: Ascarididae) in white mice and in cats. Mem Inst Oswaldo Cruz 1992; 87(4): 525-532. http://dx.doi.org/10.1590/S0074-02761992000400010. PMid:1343667.
http://dx.doi.org/10.1590/S0074-02761992...
.

Figure 1
(a) Anterior end of Lagochilascaris minor (lateral view): Post-labial groove (Pol.g) and interlabia (il). Bar = 0.04 mm; (b) Posterior end (lateral view) of male showing the ejaculatory duct (Ej.d) and spicule (sp.). Bar = 0.05 mm; (c) Egg. Bar = 0.05 mm.
Table 2
Measurements (mm) of specimens of Lagochilascaris minor, found in Leopardus geoffroyiin Rio Grande do Sul, Brazil.

Lagochilascaris minor and L. major are morphologically similar. The morphological characters that differentiate these two species are: the size of the spicules and the ejaculatory duct; and the number of sculptured pits on the surface of the eggs. In L. minor, the spicules account for 34 to 56% of the size of the ejaculatory duct, while in L. major, the spicules account for 59 to 81% of the duct size. Eggs of L. major have 35 to 45 sculptured pits, while L. minor has 15 to 25 (COSTA et al., 1986Costa HMA, Silva AVM, Costa PR, Assis SB. Lagochilascaris minor Leiper, 1909, (Nematoda-Ascaridae) de origem humana. Rev Inst Med Trop São Paulo 1986; 28(2): 126-130. http://dx.doi.org/10.1590/S0036-46651986000200009. PMid:3797950.
http://dx.doi.org/10.1590/S0036-46651986...
).

The biological cycle of L. minor has not been elucidated, but experimental models have suggested that it is heteroxenic and involves rodents and cats, as the intermediate and definitive hosts, respectively (CAMPOS et al., 1992Campos DMB, Freire Filha LG, Vieira MA, Paço JM, Maia MA. Experimental life cycle of Lagochilascaris minor Leiper, 1909. Rev Inst Med Trop São Paulo 1992; 34(4): 277-287. http://dx.doi.org/10.1590/S0036-46651992000400003. PMid:1342084.
http://dx.doi.org/10.1590/S0036-46651992...
; VOLCÁN et al., 1992Volcán GS, Medrano CE, Payares G. Experimental heteroxenous cycle of Lagochilascaris minor Leiper, 1909 (Nematoda: Ascarididae) in white mice and in cats. Mem Inst Oswaldo Cruz 1992; 87(4): 525-532. http://dx.doi.org/10.1590/S0074-02761992000400010. PMid:1343667.
http://dx.doi.org/10.1590/S0074-02761992...
; PAÇO et al., 1999Paço JM, Campos DMB, Oliveira JA. Wild rodents as experimental intermediate hosts of Lagochilascaris minor Leiper, 1909. Mem Inst Oswaldo Cruz 1999; 94(4): 441-449. http://dx.doi.org/10.1590/S0074-02761999000400003. PMid:10445999.
http://dx.doi.org/10.1590/S0074-02761999...
). Leopardus geoffroyi is an opportunistic predator and its diet may include lagomorphs, birds, insects, reptiles, amphibians and small rodents (SOUSA & BAGER, 2008Sousa KS, Bager A. Feeding habits of Geoffroy’s cat (Leopardus geoffroyi) in southern Brazil. Mamm Biol 2008; 73(4): 303-308. http://dx.doi.org/10.1016/j.mambio.2007.04.001.
http://dx.doi.org/10.1016/j.mambio.2007....
; PEREIRA et al., 2012Pereira JA, Walker RS, Novaro AJ. Effects of livestock on the feeding and spatial ecology of Geoffroy’s cat. J Arid Environ 2012; 76: 36-42. http://dx.doi.org/10.1016/j.jaridenv.2011.08.006.
http://dx.doi.org/10.1016/j.jaridenv.201...
). Its diet includes the species that have been mentioned in relation to experimental cycles of lagochilascariasis; Dasyprocta agouti (Linnaeus, 1766), D. leporine (Linnaeus, 1758), Cavia porcellus (Linnaeus, 1758) and Calomys callosus Renger, 1830 (BISCEGLIA et al., 2008Bisceglia SBC, Pereira JA, Teta P, Quintana RD. Food habits of Geoffroy’s cat (Leopardus geoffroyi) in the central Monte desert of Argentina. J Arid Environ 2008; 72(6): 1120-1126. http://dx.doi.org/10.1016/j.jaridenv.2007.11.003.
http://dx.doi.org/10.1016/j.jaridenv.200...
; SOUSA & BAGER, 2008Sousa KS, Bager A. Feeding habits of Geoffroy’s cat (Leopardus geoffroyi) in southern Brazil. Mamm Biol 2008; 73(4): 303-308. http://dx.doi.org/10.1016/j.mambio.2007.04.001.
http://dx.doi.org/10.1016/j.mambio.2007....
).

The disease appears similarly in animals and humans. It causes a granulomatous reaction of foreign-body type and lesions that are located in the tissues of the oropharynx, cervical lymph nodes, ears, paranasal sinuses, dental alveolus, lungs and brain, along with peculiar formation of fistulas in the oropharynx (PALHETA-NETO et al. 2002Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol 2002; 68(1): 101-105. http://dx.doi.org/10.1590/S0034-72992002000100018.
http://dx.doi.org/10.1590/S0034-72992002...
; BARBOSA et al., 2005Barbosa CAL, Barbosa AP, Campos DM. Gato doméstico (Felis catus domesticus) como possível reservatório de Lagochilascaris minor Leiper (1909). Rev Patol Trop 2005; 34(3): 205-211. http://dx.doi.org/10.5216/rpt.v34i3.1927.
http://dx.doi.org/10.5216/rpt.v34i3.1927...
). Other clinical signs include sinusitis, tonsillitis and respiratory and neurological manifestations that may lead to death of the animal or human (ROSEMBERG et al., 1986Rosemberg S, Lopes MBS, Masuda Z, Campos R, Bressan MCS. Fatal encephalopathy due to Lagochilascaris minor infection. Am J Trop Med Hyg 1986; 35(3): 575-578. http://dx.doi.org/10.4269/ajtmh.1986.35.575. PMid:3706624.
http://dx.doi.org/10.4269/ajtmh.1986.35....
; VELOSO et al., 1992Veloso MGP, Faria MCAR, Freitas JD, Moraes MAP, Gorini DF, Mendonça JLF. Lagoquilascaríase humana. Sobre três casos encontrados no Distrito Federal, Brasil. Rev Inst Med Trop São Paulo 1992; 34(6): 587-591. http://dx.doi.org/10.1590/S0036-46651992000600014. PMid:1342129.
http://dx.doi.org/10.1590/S0036-46651992...
). Initially, the disease is insidious, with chronic evolution and periods of remission and relapses. It is therefore difficult to diagnose and is often confused with other infections (MORAES et al., 1985Moraes MAP, Arnaud MVC, Macedo RC, Anglada AE. Infecção pulmonar fatal por Lagochilascaris sp., provavelmente Lagochilascaris minor Leiper, 1909. Rev Inst Med Trop São Paulo 1985; 27(1): 46-52. http://dx.doi.org/10.1590/S0036-46651985000100009. PMid:4035207.
http://dx.doi.org/10.1590/S0036-46651985...
; PAULA et al., 1998Paula JB, Luz JA, Barbosa CAL, Oliveira JA. Relato de um novo caso de lagochilascaríase humana procedente do sul do Pará. Rev Patol Trop 1998; 27(1): 71-76.). In the external examination performed on the L. geoffroyi specimen, no lesion was observed. At necropsy, no changes were found in the trachea and esophagus, i.e. both were intact.

Presence of lagochilascariasis in wild carnivores (Canidae and Felidae) has been recorded in Venezuela in Speothos venaticus (Lund, 1842) (VOLCAN et al., 1991Volcán GS, Medrano P, Clemencia E. Infeccion natural de Speothos venaticus (Carnivora: Canidae) por estadios adultos de Lagochilascaris sp. Rev Inst Med Trop S Paulo 1991; 33(6): 451-458. http://dx.doi.org/10.1590/S0036-46651991000600005.
http://dx.doi.org/10.1590/S0036-46651991...
); in Mexico in Puma concolor Linnaeus, 1771 (FALCÓN-ORDAZ et al., 2016Falcon-Ordáz J, Iturbe-Morgado JC, Rojas-Martínez AE, García-Prieto L. Lagochilascaris minor (Nematoda: Ascarididae) from a Wild Cougar (Puma concolor) in Mexico. J Wildl Dis 2016; 52(3): 746-748. http://dx.doi.org/10.7589/2015-09-232. PMid:27310170.
http://dx.doi.org/10.7589/2015-09-232...
); and in Argentina in Lycalopex gymnocercus (G. Fischer, 1814) (SCIOSCIA et al., 2018Scioscia NP, Olmos L, Gorosábel A, Bernad L, Pedrana J, Denegri GM. Natural infection in Pampas fox (Lycalopex gymnocercus) by Lagochilascaris major Leiper, 1910 (Nematoda: Ascarididae) in Buenos Aires, Argentina. Parasitol Res 2018; 117(9): 3023-3027. http://dx.doi.org/10.1007/s00436-018-5978-4. PMid:29938376.
http://dx.doi.org/10.1007/s00436-018-597...
).

Clinical cases in domestic cats have been reported in Uruguay (SAKAMOTO & CABRERA, 2002Sakamoto T, Cabrera PA. Subcutaneous infection of Lagochilascaris minor in domestic cats from Uruguay. Vet Parasitol 2002; 108(2): 145-152. http://dx.doi.org/10.1016/S0304-4017(02)00178-4. PMid:12208042.
http://dx.doi.org/10.1016/S0304-4017(02)...
; CASTRO et al., 2009Castro O, Venzal JM, Félix ML. Two new records of helminth parasites of domestic cat from Uruguay: Alaria alata (Goeze, 1782) (Digenea, Diplostomidae) and Lagochilascaris major Leiper, 1910 (Nematoda, Ascarididae). Vet Parasitol 2009; 160(3-4): 344-347. http://dx.doi.org/10.1016/j.vetpar.2008.11.019. PMid:19117682.
http://dx.doi.org/10.1016/j.vetpar.2008....
) and Argentina (SPRENT, 1971bSprent JFA. A Note on Lagochilascaris from the cat in Argentina. Parasitology 1971b; 63(1): 45-48. http://dx.doi.org/10.1017/S0031182000067391.
http://dx.doi.org/10.1017/S0031182000067...
). In Brazil, cases have been reported in the states of São Paulo (DELL’PORTO et al., 1988Dell’Porto A, Schumaker TTS, Oba MSP. Ocorrência de Lagochilascaris major Leiper, 1910 em gato (Felis catus domesticus L.) no Estado de São Paulo, Brazil. Rev Fac Med Vet Zootec Univ São Paulo 1988; 25(2): 173-180. http://dx.doi.org/10.11606/issn.2318-3659.v25i2p173-180.
http://dx.doi.org/10.11606/issn.2318-365...
), Rio de Janeiro (AMATO et al., 1990Amato JF, Grisi L, Pimentel M No. Two cases of fistulated abscesses caused by Lagochilascaris major in the domestic cat. Mem Inst Oswaldo Cruz 1990; 85(4): 471-473. http://dx.doi.org/10.1590/S0074-02761990000400013. PMid:2152200.
http://dx.doi.org/10.1590/S0074-02761990...
; SUDRÉ et al., 2012Sudré AP, Uchôa F, Brener B. Lagochilascariasis in a housecat and the potential risk for human disease. Braz J Infect Dis 2012; 16(1): 111-112. http://dx.doi.org/10.1016/S1413-8670(12)70289-1. PMid:22358371.
http://dx.doi.org/10.1016/S1413-8670(12)...
) and Rio Grande do Sul (REIS et al., 2011Reis RA, Mangoni CF, Mattos MJT, Marques SMT. Lagochilascaris minor (Nematoda, Ascarididae) em gato doméstico: relato de caso. Vet Foco 2011; 9(1): 43-48.; FACCIO et al., 2013Faccio L, Oliveira CB, Denardin CA, Tonin AA, Gressler LT, Dalla-Rosa L, et al. Case report: Feline infection by Lagochilascaris sp. in the State of Rio Grande do Sul, Brazil. Vet Parasitol 2013; 196(3-4): 541-543. http://dx.doi.org/10.1016/j.vetpar.2013.03.006. PMid:23582666.
http://dx.doi.org/10.1016/j.vetpar.2013....
).

A report on 13 domestic cats diagnosed with L. minor in rural areas in Pelotas (FEHLBERG et al., 2014Fehlberg MF, Silva DS, Langone PQ, Silva MAMP, Pesenti TC, Mascarenhas CS, et al. Lagochilascariasis in cats (Felis catus domesticus) in southern Brazil. J Feline Med Surg 2014; 16(12): 1007-1009. http://dx.doi.org/10.1177/1098612X14525386. PMid:24692048.
http://dx.doi.org/10.1177/1098612X145253...
) and the present report of a wild felid parasitized in an urban area suggest that presence of this parasite is possibly under diagnosed in this region. In addition, these cases serve as an alert for healthcare and animal welfare professionals regarding the pathogenic potential of this parasite, especially in relation to wild animals that are subject to anthropic pressure and live at low population densities.

Conclusions

For the first time in Brazil, L. minor is reported in L. geoffroyi. This contributes to the knowledge of the helminth fauna of this host and expands the data on the epidemiology of lagochilascariasis in the southern region of this country.

Acknowledgements

To CAPES (Brazil’s Federal Agency for the Support and Improvement of Higher Education) for its financial support. To Lázaro Luiz da Rocha Gallarraga for collect the felid for this research.

References

  • Amato JF, Grisi L, Pimentel M No. Two cases of fistulated abscesses caused by Lagochilascaris major in the domestic cat. Mem Inst Oswaldo Cruz 1990; 85(4): 471-473. http://dx.doi.org/10.1590/S0074-02761990000400013 PMid:2152200.
    » http://dx.doi.org/10.1590/S0074-02761990000400013
  • Barbosa CAL, Barbosa AP, Campos DM. Gato doméstico (Felis catus domesticus) como possível reservatório de Lagochilascaris minor Leiper (1909). Rev Patol Trop 2005; 34(3): 205-211. http://dx.doi.org/10.5216/rpt.v34i3.1927
    » http://dx.doi.org/10.5216/rpt.v34i3.1927
  • Beldomenico PM, Kinsella JM, Uhart MM, Gutierrez GL, Pereira J, Ferreyra HDV, et al. Helminths of Geoffroy’s cat, Oncifelis geoffroyi (Carnivora, Felidae) from the Monte desert, central Argentina. Acta Parasitol 2005; 50(3): 263-266.
  • Bisceglia SBC, Pereira JA, Teta P, Quintana RD. Food habits of Geoffroy’s cat (Leopardus geoffroyi) in the central Monte desert of Argentina. J Arid Environ 2008; 72(6): 1120-1126. http://dx.doi.org/10.1016/j.jaridenv.2007.11.003
    » http://dx.doi.org/10.1016/j.jaridenv.2007.11.003
  • Bowman DD, Hendrix CM, Lindsay DS, Barr SC. Feline clinical parasitology Ames: ISU Press; 2002. http://dx.doi.org/10.1002/9780470376805
    » http://dx.doi.org/10.1002/9780470376805
  • Campos DMB, Barbosa AP, Oliveira JA, Tavares GG, Cravo PVL, Ostermayer AL. Human lagochilascariasis – A rare helminthic disease. PLoS Negl Trop Dis 2017; 11(6): e0005510. http://dx.doi.org/10.1371/journal.pntd.0005510 PMid:28640884.
    » http://dx.doi.org/10.1371/journal.pntd.0005510
  • Campos DMB, Freire Filha LG, Vieira MA, Paço JM, Maia MA. Experimental life cycle of Lagochilascaris minor Leiper, 1909. Rev Inst Med Trop São Paulo 1992; 34(4): 277-287. http://dx.doi.org/10.1590/S0036-46651992000400003 PMid:1342084.
    » http://dx.doi.org/10.1590/S0036-46651992000400003
  • Castro O, Venzal JM, Félix ML. Two new records of helminth parasites of domestic cat from Uruguay: Alaria alata (Goeze, 1782) (Digenea, Diplostomidae) and Lagochilascaris major Leiper, 1910 (Nematoda, Ascarididae). Vet Parasitol 2009; 160(3-4): 344-347. http://dx.doi.org/10.1016/j.vetpar.2008.11.019 PMid:19117682.
    » http://dx.doi.org/10.1016/j.vetpar.2008.11.019
  • Costa HMA, Silva AVM, Costa PR, Assis SB. Lagochilascaris minor Leiper, 1909, (Nematoda-Ascaridae) de origem humana. Rev Inst Med Trop São Paulo 1986; 28(2): 126-130. http://dx.doi.org/10.1590/S0036-46651986000200009 PMid:3797950.
    » http://dx.doi.org/10.1590/S0036-46651986000200009
  • Dell’Porto A, Schumaker TTS, Oba MSP. Ocorrência de Lagochilascaris major Leiper, 1910 em gato (Felis catus domesticus L.) no Estado de São Paulo, Brazil. Rev Fac Med Vet Zootec Univ São Paulo 1988; 25(2): 173-180. http://dx.doi.org/10.11606/issn.2318-3659.v25i2p173-180
    » http://dx.doi.org/10.11606/issn.2318-3659.v25i2p173-180
  • Faccio L, Oliveira CB, Denardin CA, Tonin AA, Gressler LT, Dalla-Rosa L, et al. Case report: Feline infection by Lagochilascaris sp. in the State of Rio Grande do Sul, Brazil. Vet Parasitol 2013; 196(3-4): 541-543. http://dx.doi.org/10.1016/j.vetpar.2013.03.006 PMid:23582666.
    » http://dx.doi.org/10.1016/j.vetpar.2013.03.006
  • Falcon-Ordáz J, Iturbe-Morgado JC, Rojas-Martínez AE, García-Prieto L. Lagochilascaris minor (Nematoda: Ascarididae) from a Wild Cougar (Puma concolor) in Mexico. J Wildl Dis 2016; 52(3): 746-748. http://dx.doi.org/10.7589/2015-09-232 PMid:27310170.
    » http://dx.doi.org/10.7589/2015-09-232
  • Fehlberg MF, Silva DS, Langone PQ, Silva MAMP, Pesenti TC, Mascarenhas CS, et al. Lagochilascariasis in cats (Felis catus domesticus) in southern Brazil. J Feline Med Surg 2014; 16(12): 1007-1009. http://dx.doi.org/10.1177/1098612X14525386 PMid:24692048.
    » http://dx.doi.org/10.1177/1098612X14525386
  • Gallas M, Silveira EF, Perico E. Cylicospirura (Cylicospirura) felineus (Chandler, 1925) Sandground, 1932 (Nematoda, Spirocercidae) in Leopardus geoffroyi D’orbigny&Gervais, 1844 (Carnivora, Felidae): first report from the State of Rio Grande do Sul, Brazil. Neotrop Helminthol 2014; 8(2): 349-355.
  • Gallas M, Silveira EF. Mesocestoides sp. (Eucestoda, Mesocestoididae) parasitizing four species of wild felines in Southern Brazil. Rev Bras Parasitol Vet 2011; 20(2): 168-170. http://dx.doi.org/10.1590/S1984-29612011000200014 PMid:21722494.
    » http://dx.doi.org/10.1590/S1984-29612011000200014
  • Gallas M, Silveira EF. Toxocara cati (Nematoda, Ascarididae) in different wild feline species in Brazil: new host records. Biotemas 2013; 26(3): 117-125. http://dx.doi.org/10.5007/2175-7925.2013v26n3p117
    » http://dx.doi.org/10.5007/2175-7925.2013v26n3p117
  • Moraes MAP, Arnaud MVC, Macedo RC, Anglada AE. Infecção pulmonar fatal por Lagochilascaris sp., provavelmente Lagochilascaris minor Leiper, 1909. Rev Inst Med Trop São Paulo 1985; 27(1): 46-52. http://dx.doi.org/10.1590/S0036-46651985000100009 PMid:4035207.
    » http://dx.doi.org/10.1590/S0036-46651985000100009
  • Oliveira TG, Cassaro K. Guia de campo dos Felinos do Brasil São Paulo: Instituto Pró-Carnivoros, Sociedade de Zoológicos do Brasil, Fundação Parque Zoológico de São Paulo e Pró-vida Brasil; 2005.
  • Paço JM, Campos DMB, Oliveira JA. Wild rodents as experimental intermediate hosts of Lagochilascaris minor Leiper, 1909. Mem Inst Oswaldo Cruz 1999; 94(4): 441-449. http://dx.doi.org/10.1590/S0074-02761999000400003 PMid:10445999.
    » http://dx.doi.org/10.1590/S0074-02761999000400003
  • Palheta-Neto FX, Leão RNQ, Neto HF, Tomita S, Lima MAMT, Pezzin-Palheta AC. Contribuição ao estudo da lagoquilascaríase humana. Rev Bras Otorrinolaringol 2002; 68(1): 101-105. http://dx.doi.org/10.1590/S0034-72992002000100018
    » http://dx.doi.org/10.1590/S0034-72992002000100018
  • Paula JB, Luz JA, Barbosa CAL, Oliveira JA. Relato de um novo caso de lagochilascaríase humana procedente do sul do Pará. Rev Patol Trop 1998; 27(1): 71-76.
  • Pereira J, Lucherini M, Trigo T. The IUCN Red List of Treatened Species. Leopardus geoffroyi [online]. 2015 [cited 2019 June 10]. Available from: https://www.iucnredlist.org/species/15310/50657011
    » https://www.iucnredlist.org/species/15310/50657011
  • Pereira JA, Walker RS, Novaro AJ. Effects of livestock on the feeding and spatial ecology of Geoffroy’s cat. J Arid Environ 2012; 76: 36-42. http://dx.doi.org/10.1016/j.jaridenv.2011.08.006
    » http://dx.doi.org/10.1016/j.jaridenv.2011.08.006
  • Reis RA, Mangoni CF, Mattos MJT, Marques SMT. Lagochilascaris minor (Nematoda, Ascarididae) em gato doméstico: relato de caso. Vet Foco 2011; 9(1): 43-48.
  • Rosemberg S, Lopes MBS, Masuda Z, Campos R, Bressan MCS. Fatal encephalopathy due to Lagochilascaris minor infection. Am J Trop Med Hyg 1986; 35(3): 575-578. http://dx.doi.org/10.4269/ajtmh.1986.35.575 PMid:3706624.
    » http://dx.doi.org/10.4269/ajtmh.1986.35.575
  • Sakamoto T, Cabrera PA. Subcutaneous infection of Lagochilascaris minor in domestic cats from Uruguay. Vet Parasitol 2002; 108(2): 145-152. http://dx.doi.org/10.1016/S0304-4017(02)00178-4 PMid:12208042.
    » http://dx.doi.org/10.1016/S0304-4017(02)00178-4
  • Schmidt GD, Martin RL. Tapeworms of the Chaco Boreal, Paraguay, with two new species. J Helminthol 1978; 52(3): 205-209. http://dx.doi.org/10.1017/S0022149X00005381 PMid:722040.
    » http://dx.doi.org/10.1017/S0022149X00005381
  • Schmidt GD. CRC Handbook of Tapeworm identification Boca Raton: CRC Press Inc.; 1986.
  • Scioscia NP, Olmos L, Gorosábel A, Bernad L, Pedrana J, Denegri GM. Natural infection in Pampas fox (Lycalopex gymnocercus) by Lagochilascaris major Leiper, 1910 (Nematoda: Ascarididae) in Buenos Aires, Argentina. Parasitol Res 2018; 117(9): 3023-3027. http://dx.doi.org/10.1007/s00436-018-5978-4 PMid:29938376.
    » http://dx.doi.org/10.1007/s00436-018-5978-4
  • Sousa KS, Bager A. Feeding habits of Geoffroy’s cat (Leopardus geoffroyi) in southern Brazil. Mamm Biol 2008; 73(4): 303-308. http://dx.doi.org/10.1016/j.mambio.2007.04.001
    » http://dx.doi.org/10.1016/j.mambio.2007.04.001
  • Sprent JFA. Speciation and development in the genus Lagochilascaris. Parasitology 1971a; 62(1): 71-112. http://dx.doi.org/10.1017/S0031182000071316 PMid:5550315.
    » http://dx.doi.org/10.1017/S0031182000071316
  • Sprent JFA. A Note on Lagochilascaris from the cat in Argentina. Parasitology 1971b; 63(1): 45-48. http://dx.doi.org/10.1017/S0031182000067391
    » http://dx.doi.org/10.1017/S0031182000067391
  • Sudré AP, Uchôa F, Brener B. Lagochilascariasis in a housecat and the potential risk for human disease. Braz J Infect Dis 2012; 16(1): 111-112. http://dx.doi.org/10.1016/S1413-8670(12)70289-1 PMid:22358371.
    » http://dx.doi.org/10.1016/S1413-8670(12)70289-1
  • Travassos L. Contribuições para o conhecimento da fauna helmintolojica brazileira. Mem Inst Oswaldo Cruz 1917; 9(1): 5-62. http://dx.doi.org/10.1590/S0074-02761917000100001
    » http://dx.doi.org/10.1590/S0074-02761917000100001
  • Trindade MAC, Macedo MRP, Muller G. Dioctophyme renale (Nematoda: Dioctophymatidae) in Leopardus geoffroyi (Carnivora: Felidae) in the Neotropical region. Rev Bras Parasitol Vet 2018; 27(2): 223-225. http://dx.doi.org/10.1590/s1984-29612017079 PMid:29466503.
    » http://dx.doi.org/10.1590/s1984-29612017079
  • Veloso MGP, Faria MCAR, Freitas JD, Moraes MAP, Gorini DF, Mendonça JLF. Lagoquilascaríase humana. Sobre três casos encontrados no Distrito Federal, Brasil. Rev Inst Med Trop São Paulo 1992; 34(6): 587-591. http://dx.doi.org/10.1590/S0036-46651992000600014 PMid:1342129.
    » http://dx.doi.org/10.1590/S0036-46651992000600014
  • Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721(1): 1-23. http://dx.doi.org/10.11646/zootaxa.1721.1.1
    » http://dx.doi.org/10.11646/zootaxa.1721.1.1
  • Volcán GS, Medrano CE, Payares G. Experimental heteroxenous cycle of Lagochilascaris minor Leiper, 1909 (Nematoda: Ascarididae) in white mice and in cats. Mem Inst Oswaldo Cruz 1992; 87(4): 525-532. http://dx.doi.org/10.1590/S0074-02761992000400010 PMid:1343667.
    » http://dx.doi.org/10.1590/S0074-02761992000400010
  • Volcán GS, Medrano P, Clemencia E. Infeccion natural de Speothos venaticus (Carnivora: Canidae) por estadios adultos de Lagochilascaris sp. Rev Inst Med Trop S Paulo 1991; 33(6): 451-458. http://dx.doi.org/10.1590/S0036-46651991000600005
    » http://dx.doi.org/10.1590/S0036-46651991000600005

Publication Dates

  • Publication in this collection
    07 Nov 2019
  • Date of issue
    Oct-Dec 2019

History

  • Received
    20 June 2019
  • Accepted
    25 Sept 2019
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