Evaluation of Larval Development of Dirofilaria immitis in Different Populations of Aedes aegypti and Aedes albopictus

Gílcia Aparecida de Carvalho, Rafael Trindade Maia, Rafael Antonio Nascimento Ramos, Carlos Fernando Salgueirosa de Andrade, Maria Aparecida da Gloria Faustino, Leucio Câmara Alves

.
Unidade Acadêmica de Garanhuns, Universidade Federal Rural de Pernambuco, Garanhuns, Brazil.

DOI: 10.4236/ojvm.2013.36045                

Abstract

Dirofilaria immitis is an important nematode parasite commonly known as heartworm. This filarioid is transmitted by culicid vectors and primarily affects dogs, but other animals may also become infected, such as wild carnivores, cats and humans. The aim of the present study was to assess the development of D. immitis larvae in different culicid populations under laboratory conditions. Adult females of populations of Aedes aegypti from the city of Recife (P1), the city of Campinas (P2) and the Rockefeller strain from the Centers for Disease Control (P3) and one population of Aedes albopictus from Recife (P4) were fed for two hours with infected dog blood containing 2,000 microfilariae/ml of D. immitis. After artificial feeding, the specimens were maintained under controlled conditions. Ten females from each population were dissected daily over 14 days. The infection ratio and vector efficiency index were calculated and D. immitis development from L₁ to L₃ was assessed. The larvae in P1, P2, P3 and P4 reached the third stage in 11, 10, 14 and 9 days, respectively. The vector efficiency index was 53.8%, 20.0%, 7.4% and 25.2% in P1, P2, P3 and P4, respectively. The findings demonstrate that D. immitis larvae develop in all culicid populations studied herein. Based on mosquito mortality, development time and VEI the A. albopictus population from Recife (P4) demonstrated the best performance as vector. This is the second report of D. immitis development in A. albopictus from Brazil. The present data reinforce the role of this species as vector of D. immitis in an area where greater importance has long been given to A. aegypti.

Keywords

Culicid; Vector; Heartworm; Dog; Experimental Infection

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	J. W. McCall, C. Genchi, L. H. Kramer, J. Guerrero and L. Venco, “Heartworm Disease in Animals and Humans,” Advances in Parasitology, Vol. 66, No. 1, 2008, pp. 193-285. http://dx.doi.org/10.1016/S0065-308X(08)00204-2
[2]	N. Labarthe, M. L. Serrao, Y. F. Melo, S. J. Oliveira and R. Lourenco-de-Oliveira, “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, Vol. 93, No. 4, 1998, pp. 425-432. http://dx.doi.org/10.1590/S0074-02761998000400001
[3]	F. C. L. Maia, J. W. McCall, Vol. A. Silva, C. A. Peixoto, P. Supakorndej, N. Supakorndej and L. C. Alves, “Structural and Ultrastructural Changes in the Lungs of Cats Felis catus (Linnaeus, 1758) Experimentally Infected with D. immitis (Leidy, 1856),” Veterinary Parasitology, Vol. 176, No.4, 2011, pp. 304-312. http://dx.doi.org/10.1016/j.vetpar.2011.01.014
[4]	T. A. Nelson, D. G. Gregory and J. R. Laursen, “Canine Heartworms in Coyotes in Illinois,” Journal of Wildlife Diseases, Vol. 39, No. 3, 2003, pp. 593-599.
[5]	K. L. Paras, S. E. Little, M. Vol. Reichard and M. H. Reiskind, “Detection of Dirofilaria immitis and Ehrlichia Species in Coyotes (Canis latrans), from Rural Oklahoma and Texas,” Vector Borne Zoonotic Diseases, Vol. 12, No. 7, 2012, pp. 619-621. http://dx.doi.org/10.1089/vbz.2011.0815
[6]	S. Pampioglione and F. Rivasi, “Human Dirofilariasis Due to Dirofilaria (Nochtiella) repens: An Update of World Literature from 1995 to 2000,” Parassitologia, Vol. 42, No. 3-4, 2000, pp. 231-254.
[7]	R. Rodrigues-Silva, H. Moura, G. Dreyer and L. Rey, “Human Pulmonary Dirofilariasis: A Review,” Revista do Instituto de Medicina Tropical de Sao Paulo, Vol. 37, No. 6, 1995, pp. 523-530. http://dx.doi.org/10.1590/S0036-46651995000600009
[8]	K. W. Ludlam, L. A. Jachowski and G. F. Otto, “Potential VECTORS of Dirofilaria immitis,” Journal of American Mosquito Control Association, Vol. 157, No. 1, 1970, pp. 1354-1359.
[9]	G. Cancrini, P. Scaramozzino, S. Gabrielli, M. Di Paolo, L. Toma and R. Romi, “Aedes albopictus and Culex pipiens Implicated as Natural Vectors of Dirofilaria repens in Central Italy,” Journal of Medical Entomology, Vol. 44, No. 6, 2007, pp. 1064-1066. http://dx.doi.org/10.1603/0022-2585(2007)44[1064:AAACPI]2.0.CO;2
[10]	G. A. Carvalho, L. C. Alves, R. T. Maia, C. F. S. Andrade, R. A. N. Ramos and M. A. G. Faustino, “Vector Competence of Culex quinquefasciatus Say, 1823 Exposed to Different Densities of Microfilariae of Dirofilaria immitis (Leidy, 1856),” Revista Brasileira de Entomologia, Vol. 52, No. 4, 2008, pp. 658-662. http://dx.doi.org/10.1590/S0085-56262008000400018
[11]	B. M. Christensen, “Laboratory Studies on the Development and Transmission of Dirofilaria immitis by Aedes trivittatus,” Mosquito News, Vol. 37, No. 3, 1977, pp. 367-372.
[12]	M. L. C. Serrao, “Competência Vetorial de Aedes albopictus (Skuse, 1848) Proveniente do Estado do Rio de Janeiro, Brasil, para Dirofilaria immitis (Leidy, 1856) Railliet & Henry, 1911,” Ph.D. Dissertation, Universidade Federal Rural do Rio de Janeiro, Rio de Janeiro, 2004.
[13]	S. M. M. Ahid and R. Lourenco-de-Oliveira, “Mosquitos Vetores Potenciais de Dirofilariose Canina na Regiao Nordeste do Brasil,” Revista de Saúde Pública, Vol. 33, No. 6, 1999, pp. 560-565. http://dx.doi.org/10.1590/S0034-89101999000600007
[14]	W. L. Newton and W. H. Wright, “The Occurrence of a Dog Filarid Other Than Dirofilaria immitis in the United States,” Journal of Parasitology, Vol. 42, No. 3, 1956, pp. 246-258. http://dx.doi.org/10.2307/3274849
[15]	L. C. Rutledge, R. A. Ward and D. J. Gould, “Studies on the Feeding Response of Mosquitoes to Nutritive Solutions in a New Membrane Feeder,” Mosquito News, Vol. 24, No. 4, 1964, pp. 407-419.
[16]	A. E. R. Taylor, “The Development of Dirofilaria immitis the mosquito Aedes aegypti,” Journal of Helminthology, Vol. 34, No. 1-2, 1960, pp. 27-38. http://dx.doi.org/10.1017/S0022149X00020307
[17]	S. M. Ahid, P. S. Vasconcelos and R. Lourenco-de-Oliv-iera, “Vector Competence of Culex quinquefasciatus Say from Different Regions of Brazil to Dirofilaria immitis,” Memórias do Instituto Oswaldo Cruz, Vol. 95, No. 6, 2000, pp. 769-775.
[18]	L. Kartman, “Suggestions Concerning an Index Experimental Filarial Infection in Mosquitoes,” American Journal Tropical Medicine and Hygiene, Vol. 3, No. 1, 1954, pp. 329-337.
[19]	M. Ayres, M. Ayres Jr, D. L. Ayres and A. L. Santos, “BioEstat 2.0: Aplicacoes Estatísticas nas áreas das Ciências Biológicas e Médicas,” Sociedade Civil Mamirauá-CNPq, Brasília, 2000.
[20]	M. Vegni-Talluri and G. Cancrini, “An Ultrastructural Study on the Early Cellular Response to Dirofilaria immitis (Nematoda) in the Malpighian Tubules of Aedes aegypti (Refractory Strains),” Parasite, Vol. 1, No. 4, 1994, pp. 343-348.
[21]	G. A. Scoles and J. R. Craig, “Variation in Susceptibility to Dirofilaria immitis among US Strains of Aedes albopictus,” Vector Control Bulletin North Carolina States, Vol. 2, No. 1, 1993, pp. 98-103.
[22]	I. L. Mendonca, L. C. Alves, J. W. McCall, M. A. G. Faustino and P. Supakonderj, “Porcentual de Infeccao por Dirofilaria immitis (Leidy, 1856) em Aedes aegypti (Linnaeus) Através da Utilizacao de Membrana Artificial,” Ciência Veterinária nos Trópicos, Vol. 1, No. 1, 1998, pp. 30-32.
[23]	G. Cancrini, A. F. Regalbono, I. Ricci, C. Tessarin, S. Gabrielli and M. Pietrobelli, “Aedes albopictus Is a Natural Vector of Dirofilaria immitis in Italy,” Veterinary Parasitology, Vol. 118, No. 3-4, 2003, pp. 195-202. http://dx.doi.org/10.1016/j.vetpar.2003.10.011
[24]	A. H. Hawley, “The Biology of Aedes albopictus,” Journal of American Mosquito Control Association, Vol. 4, No. 2, 1988, p. e39.