Ectopic dirofilariosis in two dogs from Rio de Janeiro state, Brazil

Dirofilariose ectópica em dois cães do estado do Rio de Janeiro, Brasil

CASE REPORT

Ectopic dirofilariosis in two dogs from Rio de Janeiro state, Brazil

Dirofilariose ectópica em dois cães do estado do Rio de Janeiro, Brasil

Beatriz Brener^I; Patricia Riddell Millar^I; Danuza Pinheiro Bastos Garcia de Mattos^I; Flávia Uchôa^II; Bethânia Bastos^I; Ingrid Rodrigues Lyrio^III; Pedro Luis Aragon^III; Adriana Pittella Sudré^I

^IDepartamento de Microbiologia e Parasitologia, Universidade Federal Fluminense, RJ, Brazil

^IILaboratório Clínico Veterinário Flávia Uchôa, RJ, Brazil

^IIIClínica Veterinária Maricá, RJ, Brazil

^{Correspondence to}

SUMMARY

Report of two canine dirofilariosis cases of ectopic location in the state of Rio de Janeiro. This is the first report of erratic migration for this parasitosis in dogs in the state, calling attention to the short period of time between the two cases. The fact that the area is endemic for this parasite, its zoonotic potential and the report of human cases in the state, demonstrates that authorities should be alerted to the control programs of dirofilariosis along with the pathogenic profile of the infections.

Keywords: Dirofilariosis ectopic; Dog; Human; Dirofilaria immitis.

RESUMO

Relato de dois casos de dirofilariose canina de localização ectópica no Estado do Rio de Janeiro. Este é o primeiro relato de migração errática para esta parasitose em cães no Estado, e chama a atenção o curto espaço de tempo entre os dois casos. O fato da região ser endêmica para a parasitose, seu caráter zoonótico e o relato de casos humanos no Estado, demonstram que as autoridades competentes devem estar atentas aos programas de controle da dirofilariose assim como no perfil patogênico da infecção.

INTRODUCTION

The species Dirofilaria immitis (Leidy, 1856) is a dixenic filarid parasite that infects dogs, cats and human beings among other animal hosts^6,43. The intermediate hosts are mosquitoes from several genera, such as Culex, Aedes and Anopheles. The parasite has a worldwide distribution, and several endemic areas have been described in Brazil^{2,3,5,8,10,15,16,18,21,22,36,40} . Canids are the most adapted definitive hosts and are the primary reservoir for parasite transmission, but reports about feline and human infection are becoming more frequent, including in Brazil^{4,6,24,33,39,42}. Dirofilariosis is considered a zoonosis in human hosts since 1941, and although the parasite has been mostly described in the lungs, it has also been observed at the cardiovascular system, subcutaneous tissue, brain, testicle, eyeball, abdominal cavity and bladder^{1,14,20,24,32}. In canids, the parasite is usually found in pulmonary arteries and right ventricle, where it may cause cardiopulmonary disease²⁸. Immature adult worms may eventually migrate erroneously to unusual sites, such as the brain, liver, epidural space, anterior chamber of the eye, pericardial sac, subcutaneous tissue, bronchus and peritoneal cavity^{9,13,19,23,26,27,29,38,41,44}. Erratic migrations have also been found in the anterior chamber of the eye of dogs in Italy¹¹, Australia²⁸ and USA³⁰. Additionally, there have been some reports of migrations to the abdominal cavity^12,31. In Brazil, LENT & FREITAS (1937)²⁵ described an ectopic subcutaneous location in dogs, but the presence of D. immitis at the abdominal cavity was not observed. In a review published by BARBOSA & ALVES (2006)⁷, up to the year 2005 the Brazilian national prevalence of dirofilariosis in dogs was 10.2% based on microfilaremia and 9.1% based on circulating antigens. LABARTHE et al. (1997)²¹ observed, in Rio de Janeiro State, that 13.95% of dogs were microfilaremic and 7.98% of amicrofilaremic dogs had antigens detected by ELISA. In the same study, the region that included Maricá municipality was particularly noted for having a high prevalence, with 52.46% dogs demonstrating microfilaremia or the presence of circulating antigens. POUBEL et al. (2008)³⁵ also observed a high percentage in the same municipality, finding 33.3% of dogs infected. The aim of this study is to describe two dirofilariosis cases of ectopic location in dogs from Maricá municipality, located in the littoral area of Rio de Janeiro State.

CASE REPORTS

The first case was a 19-year-old male dog, mixed-breed, which showed no symptoms of the disease. A free immature adult inside the scrotum was observed and collected during an elective orchiectomy. The second case was a 3-year-old female dog, mixed-breed, asymptomatic, which was submitted to an elective ovariosalpingectomy. During the surgery, a free adult female approximately 20 cm in length was observed and collected inside the peritoneal cavity. The parasites were identified according to LENT & FREITAS (1937)²⁵ and FURTADO et al. (2010)¹⁷ and deposited in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC), number 35797 (whole mounts). Four months after the surgical intervention, the second animal died from distemper. During necropsy, three nematodes were observed in the abdominal region (two males measuring approximately 12 and 13 cm and one female measuring approximately 21.5 cm), three inside the pulmonary artery, and several inside the right chamber of the heart. None of the animals presented microfilariae in peripheral blood analyzed by Knott technique. The filarial antigen detection test was not performed in both cases. Both animals were previously treated with ivermectin for mange.

DISCUSSION

Since no filarial antigen detection was performed, it is not possible to assure that the first dog did not have any D. immitis in its pulmonary arteries. Regardless, the use of drugs that modify fertility of adults and that are microfilaricidal at the high dose used to treat mange, could explain the absence of microfilariae in the blood of both animals. However, it is important to note that the Knott technique is not 100% sensitive, especially in cases of low microfilaremia. According to OH et al. (2008)³¹, this parasite has been observed in several anatomic sites, but the mechanism that induces erratic migration is still unknown. OTTO (1974)³⁴ hypothesized that immature stages may occlude small vessels leading to its rupture and release of those immature adults into aberrant locations, where they may mature into adults. The fact that both animals did not have clinical symptoms, and that they were from an endemic area, reemphasizes the need for promoting control and prevention measures for this parasitosis. The geographical conditions associated with sanitary conditions, pluviometric indexes, high concentrations of mosquito populations, and the increase of dogs, cats and other errant animals populations, allow the maintenance and dissemination of D. immitis among animals and mosquitoes. This situation favors the occurrence of outbreaks and accidental cases of human infection. The ectopic location of this parasite is not commonly reported in Brazil and, although the cases reported here could be considered from an endemic area, it is important to notice that the finding of D. immitis in unusual anatomical sites is not restricted to endemic regions¹¹. Still, it is noticeable that two cases of ectopic dirofilariosis were diagnosed in dogs from the same area in a short period of time. More studies are needed to elucidate the mechanisms that drive these parasites to ectopic migrations. Additionally, many cases of canine dirofilariosis in the Maricá region have been frequently reported by veterinarians, including some of the authors, which denotes the need for control programs for this parasitosis, especially if we consider the close relationship between domestic animals and human beings, along with the zoonotic potential of this helminth, considering that cases of human dirofilariosis were already reported in the same state³⁷.

Received: 29 November 2011

Accepted: 30 March 2012

• 1. Abbas KF, El-Monem SG, Malik Z, Khan AM. Surgery still opens an unexpected bag of worms! An intraperitoneal live female Dirofilaria worm: case report and review of the literature. Surg Infect (Larchmt). 2006;7:323-5.
• 2. Ahid SMM, Lourenço-de-Oliveira R, Saraiva LQ. Dirofilariose canina na Ilha de São Luis, nordeste do Brasil: uma zoonose potencial. Cad Saude Publica.1999;15:405-12.
• 3. Alves lC, Almeida-Silva IV, Faustino MA, McCall JW, Supakonderj P, Labarthe NW, et al. Survey of canine heartworm in the city of Recife, Pernambuco, Brazil. Mem Inst Oswaldo Cruz. 1999;94:587-90.
• 4. Al-Kappany YM, Lappin MR, Kwok OC, Abu-Elwafa SA, Hilali M, Dubey JP. Seroprevalence of Toxoplasma gondii and concurrent Bartonella spp., feline immunodeficiency virus, feline leukemia virus, and Dirofilaria immitis infections in Egyptian cats. J Parasitol. 2011;97:256-8.
• 5. Araujo RT, Marcondes CB, Bastos LC, Sartor DC. Canine dirofilariasis in the region of Conceição Lagoon, Florianópolis, and in the Military Police kennel, São José, State of Santa Catarina, Brazil. Vet Parasitol. 2003;113:239-42.
• 6. Atkins CE, De Francesco TC, Coats JR, Sidley JA, Keene BW. Heartworm infections in cats: 50 cases (1985-1997). J Am Vet Med Assoc. 2000;217:355-58.
• 7. Barbosa CL, Alves LC. Dirofilariose canina: situação atual no Brasil. Rev CFMV (Brasília). 2006;12:57-62.
• 8. Brito AC, Vila-Nova MC, Rocha DAM, Gomes Costa L, Pinheiro de Almeida WA, da Silva Viana L, et al. Prevalência da filaríase canina causada por Dirofilaria immitis e Dipetalonema reconditum em Maceió, Alagoas, Brasil. Cad Saude Publica. 2001;17:1497-504.
• 9. Carastro SM, Dugan SJ, Paul AJ. Intraocular dirofilariasis in dogs. Compend Cont Educ Pract Vet.1992;14:209-17.
• 10. Costa RC, Couto-Lima D, Serrão ML, Labarthe N. An update survey of the prevalence of canine dirofilariosis in a focus area of the city of Rio de Janeiro, Brazil. Rev Bras Parasitol Vet. 2004;13:23-8.
• 11. Dantas-Torres F, Lia RP, Barbuto M, Casiraghi M, Crovace A, Caligiani L, et al. Ocular dirofilariosis by Dirofilaria immitis in a dog: first case report from Europe. J Small Anim Pract. 2009;50:667-9.
• 12. Dibbell CB. Dirofilaria immitis in abdominal cavity of dog. J Am Vet Med Ass. 1951;118:298.
• 13. Eberhard ML, Daly JJ, Weinstein S, Farris HE. Dirofilaria immitis from the eye of a dog in Arkansas. J Parasitol. 1977; 63:978.
• 14. Faust EC, Thomas ER, Jones J. Discovery of human heartworm infection in New Orleans. J Parasitol. 1941;27:115-22.
• 15. Fernandes CGN, Moura ST, Dias AR, Vieira Filho WS. Ocorrência da dirofilariose canina na região da Grande Cuiabá, Estado do Mato Grosso do Sul - Brasil. Braz J Vet Res Anim Sci. 1999; 36(5). http://dx.doi.org/10.1590/S1413-95961999000500007:00-01
• 16. Furtado AP, Do Carmo ES, Giese EG, Vallinoto ACR, Lanfredi RM, Santos JN. Detection of dog filariasis in Marajo Island, Brazil by classical and molecular methods. Parasitol Res. 2009;105:1509-15.
• 17. Furtado AP, Melo FT, Giese EG, Santos JN. Morphological redescription of Dirofilaria immitis. J Parasitol. 2010;96:499-504.
• 18. Garcez LM, Souza NF, Mota EF, Dickson LAJ, Abreu WU, Cavalcanti VFN, Gomes PAF. Focos de dirofilariose canina na Ilha do Marajó: um fator de risco para a saúde humana. Rev Soc Bras Med Trop. 2006;39:333-6.
• 19. Guterbock WM, Vestre WA, Todd KS Jr. Ocular dirofilariasis in the dog. Mod Vet Pract.1981;62:45-7.
• 20. Huang SL, Liu YH, Chen W. Subcutaneous dirofilariasis caused by Dirofilaria immitis mimicking a large epidermal cyst. J Eur Acad Dermatol Venereol. 2006;20:477-8.
• 21. Labarthe N, Almosny N, Guerrero J, Duque-Araújo AM. Description of the occurrence of canine dirofilariasis in the state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 1997; 92:47-51.
• 22. Labarthe N, Ferreira AMR, Guerrero J, Newcomb K, Paes-de-Almeida E. Survey of Dirofilaria immitis (Leidy, 1856) in random source cats in metropolitan Rio de Janeiro, Brazil, with descriptions of lesions. Vet Parasitol. 1997;71:301-6.
• 23. Lavers DW, Spratt DM, Thomas C. Dirofilaria immitis from the eye of a dog. Aust Vet J. 1969;45:284-6.
• 24. Lee ACY, Montgomery SP, Theis JH, Blagburn BL, Eberhard ML. Public health issues concerning the widespread distribution of canine heartworm disease. Trends Parasitol. 2010;26:168-73.
• 25. Lent H, Freitas JFT. Contribuição ao estudo do gênero Dirofilaria Railliet & Henry, 1911. Mem Inst Oswaldo Cruz. 1937;32:37-54.
• 26. Lent H, Freitas JFT. Dirofilariose subcutânea dos cães no Brasil. Mem Inst Oswaldo Cruz.1937;32:443-8.
• 27. Mallett G, Spratt DM, Derrington PC, Thomas C. Male Dirofilaria immitis from the eye of a dog. Aust Vet J. 1971;47:124.
• 28. McCall JW, Genchi C, Kramer LH, Guerrero J, Venco L. Heartworm disease in animals and humans. Adv Parasitol. 2008;66:193-285.
• 29. Metcalf JF, Jordan KM. Surgical removal of Dirofilaria immitis from the eye of a dog. Vet Med Small Anim Clin.1982;77:1606-8.
• 30. Miller W, Cooper RB. Identifying and treating intraocular Dirofilaria immitis in dogs. Vet Med.1987;82:381-5.
• 31. Oh HW, Jun HK, You MJ, Hayasaki M, Song KH. Ectopic migration of an adult heartworm in a dog with dirofilariasis. Korean J Parasitol. 2008;46:171-3.
• 32. Organización Mundial de La Salud. Zoonosis parasitarias. Ginebra: OMS; 1979. p. 105-6. (Informe Técnico, 637).
• 33. Otranto D, Diniz DG, Dantas-Torres F, Casiraghi M, de Almeida IN, de Almeida LN, et al. Human intraocular filariasis caused by Dirofilaria sp. nematode, Brazil. Emerg Infect Dis. 2011;17:863-6.
• 34. Otto G. Occurrence of the heartworm in unusual locations and in unusual hosts. In: Morgan HC, editor. Proceedings of the Heartworm Symposium 174. Bonner Springs, KS: UM Publishing; 1974. p. 6-8.
• 35. Poubel IT, Lima NA, Poubel R, Tebaldi FB, Pires MS, Mattos DG Jr, et al. Avaliação da influência de fatores intrínsecos na infecção por Dirofilaria immitis (Leidy, 1856) em cães do Município de Maricá, Estado do Rio de Janeiro. In: 35º Congresso Brasileiro de Medicina Veterinária; 2008. p. 1-6.
• 36. Reifur L,Thomaz-Socco lV, Montiani-Ferreira F. Epidemiological aspects of filariosis in dogs on the coast of Paraná State, Brazil: with emphasis on Dirofilaria immits Vet Parasitol. 2004;122:273-86.
• 37. Rodrigues-Silva R, Guerra RJA, Almeida FB, Machado-Silva JR, Paiva DD. Dirofilaríase pulmonar humana no Estado do Rio de Janeiro, Brasil: relato de um caso. Rev Soc Bras Med Trop. 2004;37:56-9.
• 38. Sevimli FK, Kozan E, Bülbül A, Birdane FM, Köse M, Sevimli A. Dirofilaria immitis infection in dogs: unusually located and unusual findings. Parasitol Res. 2007;101:1487-94.
• 39. Silva RC, Langoni H. Dirofilariose: zoonose emergente negligenciada. Cienc Rural. 2009;39:1614-23.
• 40. Souza NF, Larsson MHMA. Frequency of canine heartworm disease (D. immitis) in some regions of São Paulo State using a circulating antigen indicator test. Arq Bras Med Vet Zootec. 2001;53:321-5.
• 41. Thornton JG. Heartworm invasion of the canine eye. Mod Vet Pract.1978;59:373-4.
• 42. Traversa D, Aste G, Milillo P, Capelli G, Pampurini F, Tunesi C, et al. Autochthonous foci of canine and feline infections by Dirofilaria immitis and Dirofilaria repens in central Italy. Vet Parasitol. 2010;169(1-2):128-32.
• 43. Vital RJ, Mattos, LA, Meirelles GS. Human pulmonary dirofilariasis: atypical presentation of a rare disease. Rev Soc Bras Med Trop. 2006;39:94-5.
• 44. Venco L, Kramer L, Genchi C. Heartworm disease in dogs: unusual clinical cases. Vet Parasitol. 2005;133:207-18.

Publication Dates

• Publication in this collection
  21 May 2012
• Date of issue
  June 2012

History

• Received
  29 Nov 2011
• Accepted
  30 Mar 2012