Canine heartworm: natural infection along remote coastal area of Rio de Janeiro

Main Article Content

Mário dos Santos Filho
Bruno Alberigi
Debora Macedo Pedroso Balius
Nathália Marques de Oliveira Lemos
Alexandre José Rodrigues Bendas
Jonimar Pereira Paiva

Abstract

Dirofilaria immitis is a mosquito-borne nematode that often infects dogs worldwide and causes what is commonly referred to as heartworm disease. The infection is recognized as being more prevalent in tropical and subtropical coastal regions; however, due to recent climate changes, it has been detected in regions previously considered free of infection. The asymptomatic animals presented in this case report had their infections detected opportunistically. One was presented for a routine checkup and the other for pre-operative evaluation. In the checkup case, heartworm disease was suspected after auscultation. In the presurgical case, microfilariae were found when cytology was performed. Both dogs had D. immitis infection confirmed by antigen detection using an enzyme-linked immunosorbent assay (ELISA) test. The microfilariae were confirmed to be D. immitis. This report highlights the unsuspected finding of the infection in a region where canine heartworm disease has not been a concern. It throws light on the importance of constant surveillance of animal vector-borne diseases in areas of ecotone. Surveillance must be reinforced when natural resources are disturbed, especially in the face of global climate change.

Article Details

How to Cite
dos Santos Filho, M. ., Alberigi, B. ., Macedo Pedroso Balius, D. ., Marques de Oliveira Lemos, N. ., Rodrigues Bendas, A. J. ., & Pereira Paiva, J. (2021). Canine heartworm: natural infection along remote coastal area of Rio de Janeiro. Brazilian Journal of Veterinary Medicine, 43(1), e000220. https://doi.org/10.29374/2527-2179. bjvm000220
Section
Case report

References

Ahid, S. M. M., & Lourenço-de-Oliveira, R. (1999). Mosquitos vetores potenciais de dirofilariose canina na Região Nordeste do Brasil. Revista de Saúde Pública, 33(6), 560-565. http://dx.doi.org/10.1590/S0034- 89101999000600007. PMid:10689372.

Alberigi, B., Fernandes, J. I., Paiva, J. P., Mendes-de-Almeida, F., Knackfuss, F., Merlo, A., & Labarthe, N. (2020). Efficacy of semi-annual therapy of an extended-release injectable moxidectin suspension and oral doxycycline in Dirofilaria immitis naturally infected dogs. Parasites & Vectors, 13(1), 503. http://dx.doi.org/10.1186/s13071- 020-04380-z. PMid:33023664.

Alirol, E., Getaz, L., Stoll, B., Chappuis, F., & Loutan, L. (2011). Urbanisation and infectious diseases in a globalised world. The Lancet. Infectious Diseases, 11(2), 131-141. http://dx.doi.org/10.1016/S1473-3099(10)70223-1. PMid:21272793.

American Heartworm Society. (2020). Current Canine Guidelines for the Prevention, Diagnosis and Management of Heartworm (Dirofilaria immitis) Infection in Dogs. https://d3ft8sckhnqim2.cloudfront.net/images/ pdf/2020_AHS_Canine_Guidelines.pdf?1580934824

Atwell, R. B., Sutton, R. H., & Moodie, E. W. (1988). Pulmonary changes associated with dead filariae (Dirofilaria immitis) and concurrent antigenic exposure in dogs. Journal of Comparative Pathology, 98(3), 349-361. http:// dx.doi.org/10.1016/0021-9975(88)90043-6. PMid:3392249.

Backer, L. C., & Miller, M. (2016). Sentinel animals in a one health approach to harmful cyanobacterial and algal blooms. Veterinary Sciences, 3(2), 8. http://dx.doi.org/10.3390/vetsci3020008. PMid:27152315.

Bendas, A. J. R., Branco, A. S., da Silva, B. R. S. A., Paiva, J. P., de Miranda, M. G. N., Mendes-de-Almeida, F., & Labarthe, N. V. (2019). Mosquito abundance in a Dirofilaria immitis hotspot in the eastern state of Rio de Janeiro, Brazil. Veterinary Parasitology. Regional Studies and Reports, 18, 100320. http://dx.doi.org/10.1016/j. vprsr.2019.100320. PMid:31796177.

Bowman, D. D., & Atkins, C. E. (2009). Heartworm biology, treatment, and control. Veterinary Clinical Small Animal Practice, 39(6), 1127-1158. http://dx.doi.org/10.1016/j.cvsm.2009.06.003. PMid:19932367.

Campbell-Lendrum, D., Manga, L., Bagayoko, M., & Sommerfeld, J. (2015). Climate change and vector-borne diseases: What are the implications for public health research and policy? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 370(1665), e20130552. http://dx.doi.org/10.1098/ rstb.2013.0552. PMid:25688013.

Cancrini, G., Di Regalbono, A. F., Ricci, I., Tessarin, C., Gabrielli, S., & Pietrobelli, M. (2003). Aedes albopictus is a natural vector of Dirofilaria immitis in Italy. Veterinary Parasitology, 118(3-4), 195-202. http://dx.doi.org/10.1016/j. vetpar.2003.10.011. PMid:14729167.

Carvalho, S. C., Martins-Junior, A. J., Lima, J. B., & Valle, D. (2002). Temperature influence on embryonic development of Anopheles albitarsis and Anopheles aquasalis. Memórias do Instituto Oswaldo Cruz, 97(8), 1117-1120. http://dx.doi.org/10.1590/S0074-02762002000800009. PMid:12563476.

Christensen, B. M., & Hollander, A. L. (1978). Effect of temperature on vector-parasite relationships of Aedes trivittatus and Dirofilaria immitis. Proceedings of the Helminthological Society of Washington, 45, 115-119.

Comiskey, N & Wesson, D. M. (1995). Dirofilaria (Filarioidea: Onchocercidae) Infection in Aedes albopictus (Diptera: Culicidae) Collected in Louisiana. Journal of Medical Entomology, 32(5):734–737. https://doi.org/10.1093/ jmedent/32.5.734.

Farias, H. S., Vargas, K. B., Marino, T. B., Sousa, G. M., & Lucena, A. J. (2020). Vulnerabilidade socioambiental no Oeste Metropolitano do Rio de Janeiro: estratégias de prevenção a riscos. Revista Brasileira de Geografia Econômica, 9(19), e2020. http://dx.doi.org/10.4000/espacoeconomia.14182.

Ferreira, A. F., Barbosa, F. C., & Mastrantonio, E. C. (1999). Ocorrência da dirofilariose canina na cidade de Uberlândia, MG, Brasil. Veterinaria Noticias, 5(1), 57-61.

Genchi, C., & Kramer, L. H. (2020). The prevalence of Dirofilaria immitis and Dirofilaria repens in the Old World. Veterinary Parasitology, 280, e108995. http://dx.doi.org/10.1016/j.vetpar.2019.108995. PMid:32155518.

Grapatsas, K., Kayser, G., Passlick, B., & Wiesemann, S. (2018). Pulmonary coin lesion mimicking lung cancer reveals an unexpected finding: Dirofilaria immitis. Journal of Thoracic Disease, 10(6), 3879-3882. http://dx.doi. org/10.21037/jtd.2018.05.137. PMid:30069389.

Gratz, N. G. (2004). Critical review of the vector status of Aedes albopictus. Medical and Veterinary Entomology, 18(3), 215-227. http://dx.doi.org/10.1111/j.0269-283X.2004.00513.x. PMid:15347388.

Knight, D. H., & Lok, J. B. (1998). Seasonality of heartworm infection and implications for chemoprophylaxis. Clinical Technology Small Animals, 13(2), 77-82. http://dx.doi.org/10.1016/S1096-2867(98)80010-8. PMid:9753795.

Labarthe, N. V., Almosny, N., Guerrero, J., & Duque-Araújo, A. M. (1997). Description of the occurrence of canine dirofilariasis in the State of Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz, 92(1), 47-51. http:// dx.doi.org/10.1590/S0074-02761997000100010. PMid:9302414.

Labarthe, N. V., Paiva, J. P., Reifur, L., Mendes-de-Almeida, F., Merlo, A., Pinto, C. J. C., & Alves, L. C. (2014). Updated canine infection rates for Dirofilaria immitis in areas of Brazil previously identified as having a high incidence of heartworm-infected dogs. Parasites & Vectors, 7(1), 493. http://dx.doi.org/10.1186/s13071- 014-0493-7. PMid:25376238.

Labarthe, N. V., Serrão, M. L., Melo, Y. F., Oliveira, S. J., & Lourenço-de-Oliveira, R. (1998a). Potential vectors of Dirofilaria immitis (Leidy, 1856) in Itacoatiara, Oceanic Region of Niterói Municipality, State of Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz, 93(4), 425-432. http://dx.doi.org/10.1590/S0074-02761998000400001. PMid:9711329.

Labarthe, N. V., Serrão, M. L., Melo, Y. F., Oliveira, S. J., & Lourenço-de-Oliveira, R. (1998b). Mosquito frequency and feeding habits in an enzootic canine dirofilariasis area in Niterói, state of Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz, 93(2), 145-154. http://dx.doi.org/10.1590/S0074-02761998000200002. PMid:9698883.

Ledesma, N., & Harrington, L. (2011). Mosquito vectors of dog heartworm in the united states: vector status and factors influencing transmission efficiency. Topics in Companion Animal Medicine, 26(4), 178-185. http://dx.doi. org/10.1053/j.tcam.2011.09.005. PMid:22152605.

Lohmann, U., Sausen, R., Bengtsson, L., Cubasch, U., Perlwitz, J., & Roeckner, E. (1993). The Köppen climate classification as a diagnostic tool for general circulation models. Climate Research, 3, 177-193. http://dx.doi. org/10.3354/cr003177.

Lourenço-de-Oliveira, R., & Deane, L. M. (1995). Presumed Dirofilaria irnrnitis Infections in Wild-Caught Aedes taeniorhynchus and Aedes scapularis in Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz, 90(3), 387-388. http://dx.doi.org/10.1590/S0074-02761995000300013. PMid:8544737.

Macêdo, F. C., Labarthe, N., & Lourenço-de-Oliveira, R. (1998). Susceptibility of Aedes scapularis (Rondani, 1848) to Dirofilaria immitis (Leidy, 1856), an Emerging Zoonosis. Memórias do Instituto Oswaldo Cruz, 93(4), 435-437. http://dx.doi.org/10.1590/S0074-02761998000400003. PMid:9711331.

Magi, M., Calderini, P., Gabrielli, S., Dell’Omodarme, M., Macchioni, F., Prati, M. C., & Cancrini, G. (2008). Vulpes vulpes: A possible wild reservoir for zoonotic filariae. Vector Borne and Zoonotic Diseases (Larchmont, N.Y.), 8(2), 249-252. http://dx.doi.org/10.1089/vbz.2007.0207. PMid:18260788.

McCall, J. W. (2005). The safety-net story about macrocyclic lactone heartworm preventives: a review, an update, and recommendations. Veterinary Parasitology, 133(2-3), 197-206. http://dx.doi.org/10.1016/j.vetpar.2005.04.005. PMid:16198822.

Milanez-de-Campos, J. R., Barbas, C. S., Filomeno, L. T., Fernandez, A., Minamoto, H., Filho, J. V., & Jatene, F. B. (1997). Human pulmonary dirofilariasis: Analysis of 24 cases from São Paulo, Brazil. Chest, 112(3), 729-733. http://dx.doi.org/10.1378/chest.112.3.729. PMid:9315807.

Mitchell, C. J. (1995). Geographic spread of Aedes albopictus and potential for involvment in arbovirus cycles in the mediterranean basin. Journal of Vector Ecology, 20, 44-58.

Nayar, J. K., & Knight, J. W. (1999). Aedes albopictus (Diptera: Culicidae): an experimental and natural host of Dirofilaria immitis (Filarioidea: Onchocercidae) in Florida, U.S.A. Journal of Medical Entomology, 36(4), 441- 448. http://dx.doi.org/10.1093/jmedent/36.4.441. PMid:10467770.

Penezić, A., Selakovic, S., Pavlovic, I., & Cirovic, D. (2014). First findings and prevalence of adult heartworms (Dirofilaria immitis) in wild carnivores from Serbia. Parasitology Research, 113(9), 3281-3285. http://dx.doi. org/10.1007/s00436-014-3991-9. PMid:24951168.

Racloz, V., Griot, C., & Stärk, K. D. C. (2006). Sentinel surveillance systems with special focus on vector-borne diseases. Animal Health Research Reviews, 7(1-2), 71-79. http://dx.doi.org/10.1017/S1466252307001120. PMid:17389055.

Rozanski, E. A. (2020). Canine Chronic Bronchitis: a update. Veterinary Clinics: Small Animal Practice, 44(1):107- 116. https://doi.org/10.1016/j.cvsm.2013.09.005.

Sanavria, A., Silva, C., Electo, É. H., Nogueira, L., Thomé, S., Angelo, I., Vita, G. F., Sanavria, T., Padua, E. D., & Gaiotte, D. G. (2017). Intelligent monitoring of Aedes aegypti in a rural area of Rio de Janeiro State, Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 59(0), e51. http://dx.doi.org/10.1590/s1678-9946201759051. PMid:28793020.

Schmidt, P. L. (2009). Companion animals as sentinels for public health. The Veterinary Clinics of North America. Small Animal Practice, 39(2), 241-250. http://dx.doi.org/10.1016/j.cvsm.2008.10.010. PMid:19185191.

Serrão, M. L., Labarthe, N. V., & Lourenço-de-Oliveira, R. (2001). Vectorial Competente of Aedes aegypti (Linnaeus 1762) Rio de Janeiro Strain, to Dirofilaria immitis (Leidy 1856). Memórias do Instituto Oswaldo Cruz, 96(5), 593-598. http://dx.doi.org/10.1590/S0074-02762001000500001. PMid:11500754.

Silva, P. C. B., Oliveira-Junior, R. R., & Borges, M. S. (2020). Scenarios of territorial inequalities in the Brazil: A study on Baixada Fluminense (RJ). Brazilian Journal of Development, 6(9), 72767-72779. http://dx.doi.org/10.34117/ bjdv6n9-648.

Traversa, D., Aste, G., Milillo, P., Capelli, G., Pampurini, F., Tunesi, C., Santori, D., Paoletti, B., & Boari, A. (2010). Autochthonous foci of canine and feline infections by Dirofilaria immitis and Dirofilaria repens in central Italy. Veterinary Parasitology, 169(1-2), 128-132. http://dx.doi.org/10.1016/j.vetpar.2009.12.034. PMid:20097479.

Trotti, G. C., Pampiglione, S., & Rivasi, F. (1997). The species of the genus Dirofilaria Railliet & Henry, 1911. Parasitologia, 39(4), 369-374. PMid:9802094.