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Development of Acanthocheilonema reconditum (Spirurida, Onchocercidae) in the cat flea Ctenocephalides felis (Siphonaptera, Pulicidae)

Published online by Cambridge University Press:  28 July 2014

ETTORE NAPOLI
Affiliation:
Dipartimento di Scienze Veterinarie, Università degli Studi di Messina, Messina, Italy
EMANUELE BRIANTI*
Affiliation:
Dipartimento di Scienze Veterinarie, Università degli Studi di Messina, Messina, Italy
LUIGI FALSONE
Affiliation:
Dipartimento di Scienze Veterinarie, Università degli Studi di Messina, Messina, Italy
GABRIELLA GAGLIO
Affiliation:
Dipartimento di Scienze Veterinarie, Università degli Studi di Messina, Messina, Italy
SABRINA FOIT
Affiliation:
Bayer Animal Health GmbH (BAH), Monheim, Germany
FRANCESCA ABRAMO
Affiliation:
Dipartimento di Patologia Animale, Università di Pisa, Pisa, Italy
GIADA ANNOSCIA
Affiliation:
Dipartimento di Medicina Veterinaria, Università di Bari, Valenzano, Bari, Italy
FILIPE DANTAS-TORRES
Affiliation:
Dipartimento di Medicina Veterinaria, Università di Bari, Valenzano, Bari, Italy Department of Immunology, Aggeu Magalhães Research Centre, Oswaldo Cruz Foundation, Recife, Pernambuco 50670420, Brazil
SALVATORE GIANNETTO
Affiliation:
Dipartimento di Scienze Veterinarie, Università degli Studi di Messina, Messina, Italy
DOMENICO OTRANTO
Affiliation:
Dipartimento di Medicina Veterinaria, Università di Bari, Valenzano, Bari, Italy
*
* Corresponding author: Dipartimento di Scienze Veterinarie, Università degli Studi di Messina, Polo Universitario dell'Annunziata, 98168, Messina, Italy. E-mail: [email protected]

Summary

To investigate larval development of Acanthocheilonema reconditum in the cat flea Ctenocephalides felis, fleas were fed through an artificial feeding system with dog blood containing different concentrations of microfilariae (i.e. low, group L = 250; medium, group M = 500; high, group H = 1500 microfilariae per mL) or no microfilariae (group C). Fleas were sampled at 12 different time-points throughout the study period (D1–D28) and A. reconditum was detected by dissection, PCR and histology. Of 2105 fleas fed with infected dog blood, 891 (38·7%) died during the study before being sampled whilst the remaining (n = 1214) were examined for A. reconditum. Upon dissection, first-stage larvae (L1) were identified after 2 days post infection (D2), second-stage (L2) at D13 and infective third-stage larvae (L3) at D15. Eighteen (30%) of 60 pools of fleas molecularly examined tested positive. Histologically, L2 were detected at D13 in the sub-cuticle region embedded in the back muscle of one female flea. This study provides original data on larval development of A. reconditum in C. felis and reports on the usefulness of the artificial feeding system.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 33893402.CrossRefGoogle ScholarPubMed
Alves, L. C., de Almeida Silva, L. V., Faustino, M. A., McCall, J. W., Supakonderj, P., Labarthe, N. W., Sanchez, M. and Caires, O. (1999). Survey of canine heartworm in the city of Recife, Pernambuco, Brazil. Memorial Instituto Oswaldo Cruz 94, 587590.CrossRefGoogle ScholarPubMed
Aranda, C., Panyella, O., Eritja, R. and Castella, J. (1998). Canine filariasis. Importance and transmission in the Baix Lobregat area, Barcelona (Spain). Veterinary Parasitology 77, 267275.CrossRefGoogle Scholar
Bain, O. and Beaucournu, J. C. (1974). Larves infestantes de Dipetalonema sp. chez des puces récoltées chez des renards du sud-ouest de la France. Annales de Parasitologie 49, 123125.Google Scholar
Boreham, R. E. and Boreham, P. F. L. (1990). Dipylidium caninum: life cycle, epizootiology, and control. Compendium on Continuing Education for the Practicing Veterinarian 12, 667675.Google Scholar
Bouhsira, E., Ferrandez, Y., Liu, M., Franc, M., Boulouis, H. J. and Biville, F. (2013). Ctenocephalides felis an in vitro potential vector for five Bartonella species. Comparative Immunology, Microbiology and Infectious Diseases 36, 105111.CrossRefGoogle Scholar
Brianti, E., Otranto, D., Dantas-Torres, F., Weigl, S., Latrofa, M. S., Gaglio, G., Napoli, E., Brucato, G., Cauquil, L., Giannetto, S. and Bain, O. (2011). Rhipicephalus sanguineus (Ixodida, Ixodidae) as intermediate host of a canine neglected filarial species with dermal microfilariae. Veterinary Parasitology 183, 330337.CrossRefGoogle ScholarPubMed
Brianti, E., Gaglio, G., Napoli, E., Giannetto, S., Dantas-Torres, F., Bain, O. and Otranto, D. (2012). New insights into the ecology and biology of Acanthocheilonema reconditum (Grassi, 1889) causing canine subcutaneous filariosis. Parasitology 139, 530536.CrossRefGoogle ScholarPubMed
Calandruccio, S. (1892). Descrizione degli embrioni e delle larve della Filaria recondita (Grassi). Atti dell'Accademia Gioenia di Scienze Naturali in Catania V, Serie 4a – Mem. I. 115.Google Scholar
Casiraghi, M., Bain, O., Guerrero, R., Martin, C., Pocacqua, V., Gardner, S. L., Franceschi, A. and Bandi, C. (2004). Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. International Journal for Parasitology 34, 191203.CrossRefGoogle ScholarPubMed
Cringoli, G., Rinaldi, L., Veneziano, V. and Capelli, G. (2001). A prevalence survey and risk analysis of filariosis in dogs from the Mt. Vesuvius area of southern Italy. Veterinary Parasitology 13, 243252.CrossRefGoogle Scholar
Dryden, M. W. (1989). Host association, on-host longevity and egg production of Ctenocephalides felis felis . Veterinary Parasitology 34, 117122.CrossRefGoogle ScholarPubMed
Dryden, M. W. (1993). Biology of fleas of dogs and cats. Compendium on Continuing Education for the Practicing Veterinarian 15, 569579.Google Scholar
Dryden, M. W. and Gaafar, S. M. (1991). Blood consumption by the cat flea, Ctenocephalides felis (Siphonaptera: Pulicidae). Journal of Medical Entomology 28, 394400.CrossRefGoogle ScholarPubMed
Duke, B. O. (1962). Studies on factors influencing the transmission of onchocerciasis. I. The survival rate of Simulium damnosum under laboratory conditions and the effect upon it of Onchocerca volvulus . Annals Tropical Medicine and Parasitology 56, 130135.CrossRefGoogle ScholarPubMed
Eisen, R. J. and Gage, K. L. (2012). Transmission of flea-borne zoonotic agents. Annual Review of Entomology 57, 6182.CrossRefGoogle ScholarPubMed
Eisen, R. J., Wilder, A. P., Bearden, S. W., Montenieri, J. A. and Gage, K. L. (2007). Early-phase transmission of Yersinia pestis by unblocked Xenopsylla cheopis (Siphonaptera: Pulicidae) is as efficient as transmission by blocked fleas. Journal of Medical Entomology 44, 678682.CrossRefGoogle ScholarPubMed
Fahrner, J. and Barthelmess, C. (1988). Rearing of Culicoides nubeculosus (Diptera: Ceratopogonidae) by natural and artificial feeding in the laboratory. Veterinary Parasitology 28, 307313.CrossRefGoogle ScholarPubMed
Farnell, D. R. and Faulkner, D. R. (1978). Prepatent period of Dipetalonema reconditum in experimentally infected dogs. Journal of Parasitology 64, 565567.CrossRefGoogle ScholarPubMed
Fourie, J. J., Crafford, D., Horak, I. G. and Stanneck, D. (2012). Prophylactic treatment of flea-infested cats with an imidacloprid/flumethrin collar to forestall infection with Dipylidium caninum . Parasites and Vectors 27, 151.CrossRefGoogle Scholar
Giannetto, S., Poglayen, G., Gaglio, G. and Brianti, E. (2007). Prevalence and epidemiological aspects of microfilaraemia in dogs in Sicily. Abstract book of the 1st European Dirofilaria days, Zagreb, Croatia, February 22–25, 2007.Google Scholar
Grassi, B. and Calandruccio, S. (1890). Über haematozoon lewis entwiklungscyclus einer filaria (F. recondita) des hudes. Central Bakt Parasitenk Infectionsk 7, 816.Google Scholar
Hastriter, M. W. and Cavanaugh, D. C. (1981). An apparatus for colonizing fleas (Siphonaptera) and collecting pupal cocoons. Journal of Medical Entomology 18, 251252.CrossRefGoogle Scholar
Hastriter, M. W., Robinson, D. M. and Cavanaugh, D. C. (1980). An improved apparatus for safely feeding fleas (Siphonaptera) in plague studies. Journal of Medical Entomology 17, 387388.CrossRefGoogle Scholar
Hornok, S., Meli, M. L., Perreten, A., Farkas, R., Willi, B., Beugnet, F., Lutz, H. and Hofmann-Lehmann, R. (2010). Molecular investigation of hard ticks (Acari: Ixodidae) and fleas (Siphonaptera: Pulicidae) as potential vectors of rickettsial and mycoplasmal agents. Veterinary Microbiology 140, 98104.CrossRefGoogle ScholarPubMed
Hunt, G. J. and McKinnon, C. N. (1990). Evaluation of membranes for feeding Culicoides variipennis (Diptera: Ceratopogonidae) with an improved artificial blood-feeding apparatus. Journal of Medical Entomology 27, 934937.CrossRefGoogle ScholarPubMed
Hurd, H. (2003). Manipulation of medically important insect vectors by their parasites. Annual Review of Entomology 48, 141161.CrossRefGoogle ScholarPubMed
Husain, A. and Kershaw, W. E. (1971). The effect of filariasis on the ability of a vector mosquito to fly and feed and to transmit the infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 617619.CrossRefGoogle ScholarPubMed
Ismaeel, A. Y., Garmson, J. C., Molyneux, D. H. and Bates, P. A. (1998). Transformation, development, and transmission of axenically cultured amastigotes of Leishmania mexicana in vitro and in Lutzomyia longipalpis . American Journal of Tropical Medicine and Hygiene 59, 421425.CrossRefGoogle ScholarPubMed
Kernif, T., Leulmi, H., Socolovschi, C., Berenger, J. M., Lepidi, H., Bitam, I., Rolain, J. M., Raoult, D. and Parola, P. (2014). Acquisition and excretion of Bartonella quintana by the cat flea, Ctenocephalides felis felis . Molecular Ecology 23, 12041212.CrossRefGoogle ScholarPubMed
Kershaw, W. E., Lavoipierre, M. M. and Chalmers, T. A. (1953). Studies on the intake of microfilariae by their insect vectors, their survival, and their effect on the survival of their vectors. I. Dirofilaria immitis and Aedes aegypti . Annals of Tropical Medicine and Parasitology 47, 207224.CrossRefGoogle ScholarPubMed
Kogan, P. H. (1990). Substitute blood meal for investigating and maintaining Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 27, 709712.CrossRefGoogle ScholarPubMed
Korkejian, A. and Edeson, J. F. (1978). Studies on naturally occurring filarial infections in dogs in Lebanon. I. Dipetalonema reconditum . Annals of Tropical Medicine and Parasitology 72, 6578.CrossRefGoogle ScholarPubMed
Lappin, M. R., Davis, W. L., Hawley, J. R., Brewer, M., Morris, A. and Stanneck, D. (2013). A flea and tick collar containing 10% imidacloprid and 4·5% flumethrin prevents flea transmission of Bartonella henselae in cats. Parasites and Vectors 6, 26.CrossRefGoogle ScholarPubMed
Latrofa, M. S., Weigl, S., Dantas-Torres, F., Annoscia, G., Traversa, D., Brianti, E. and Otranto, D. (2012). A multiplex PCR for the simultaneous detection of species of filarioids infesting dogs. Acta Tropica 122, 150154.CrossRefGoogle ScholarPubMed
Lindemann, B. A. and McCall, J. W. (1984). Experimental Dipetalonema reconditum infections in dogs. Journal of Parasitology 70, 167168.CrossRefGoogle ScholarPubMed
Macaluso, K. R., Pornwiroon, W., Popov, V. L. and Foil, L. D. (2008). Identification of Rickettsia felis in the salivary glands of cat fleas. Vector-Borne and Zoonotic Diseases 3, 391396.CrossRefGoogle Scholar
Mazzotti, L. and Chabaud, A. G. (1962). Presence of Dipetalonema reconditum in dogs in Mexico. Annales de Parasitologie Humaine et Comparée 37, 673674.CrossRefGoogle ScholarPubMed
Minnaar, W. N. and Krecek, R. C. (2001). Helminths in dogs belonging to people in a resource-limited urban community in Gauteng, South Africa. Onderstepoort Journal of Veterinary Research 68, 111117.Google Scholar
Morick, D., Krasnov, B. R., Khokhlova, I. S., Gutiérrez, R., Fielden, L. J., Gottlieb, Y. and Harrus, S. (2013). Effects of Bartonella spp. on flea feeding and reproductive performance. Applied Environmental Microbiology 79, 34383443.CrossRefGoogle ScholarPubMed
Nelson, G. S. (1962). Dipetalonema reconditum (Grassi, 1889) from the dog with a note on its development in the fleas. Journal of Entomology 35, 149160.Google Scholar
Newton, W. L. and Wright, W. H. (1959). The occurrence of the dog filariid other than Dirofilaria immitis in the USA. Journal of Parasitology 43, 589.CrossRefGoogle Scholar
Olmenga-Garcìa, A. S., Rodrìguez-Rodrìguez, J. A. and Rojo-Vàzques, F. A. (1993). Experimental transmission of Dipetalonema dracunculoides (Cobbold 1870) by Rhipicephalus sanguineus (Latreille 1806). Veterinary Parasitology 47, 339342.CrossRefGoogle Scholar
Ortega-Mora, L. M., Gomez-Bautista, M., Rojo-Vazquez, F., Rodenas, A. and Guerrero, J. (1991). A survey of the prevalence of canine filariasis in Spain. Preventive Veterinary Medicine 11, 6368.CrossRefGoogle Scholar
Osbrink, W. L. A. and Rust, M. K. (1984). Fecundity and longevity of the adult cat flea, Ctenocephalides felis felis (Siphonaptera: Pulicidae). Journal of Medical Entomology 21, 727731.CrossRefGoogle Scholar
Otranto, D., Dantas-Torres, F., Brianti, E., Traversa, D., Petrić, D., Genchi, C. and Capelli, G. (2013). Vector-borne helminths of dogs and humans in Europe. Parasites and Vectors 6, 16.CrossRefGoogle ScholarPubMed
Pampiglione, S., Poglayen, G. and Capelli, G. (1986). Distribuzione geografica delle filariosi canine in Italia. Parassitologia 28, 297300.Google Scholar
Pennington, N. E. (1971). Arthropod vectors, cyclodevelopment and prepatent period of Dipetalonema reconditum (Grassi) and the incidence of canine filariasis and ectoparasite in north-central Oklahoma. Unpublished Ph.D. thesis. Oklahoma State University, Stillwater, OK, USA.Google Scholar
Pennington, N. E. and Phelps, C. A. (1969). Canine filariasis on Okinawa, Ryukyu Islands. Journal of Medical Entomology 6, 5967.CrossRefGoogle ScholarPubMed
Ramos, R. A., Giannelli, A., Brianti, E., Annoscia, G., Cantacessi, C., Dantas-Torres, F. and Otranto, D. (2013). Tick vectors of Cercopithifilaria bainae in dogs: Rhipicephalus sanguineus sensu lato versus Ixodes ricinus . Parasitology Research 112, 30133017.CrossRefGoogle ScholarPubMed
Rebeil, R., Jarrett, C. O., Driver, J. D., Ernst, R. K., Oyston, P. C. and Hinnebusch, B. J. (2013). Induction of the Yersinia pestis PhoP-PhoQ regulatory system in the flea and its role in producing a transmissible infection. Journal of Bacteriology 195, 19201930.CrossRefGoogle ScholarPubMed
Reif, K. E., Kearney, M. T., Foil, L. D. and Macaluso, K. R. (2011). Acquisition of Rickettsia felis by cat fleas during feeding. Vector Borne Zoonotic Disease 11, 963968.CrossRefGoogle ScholarPubMed
Richman, D. L., Koehler, P. G. and Brenner, R. J. (1999). Spray-dried bovine blood: an effective laboratory diet for Ctenocephalides felis felis (Siphonaptera: Pulicidae). Journal of Medical Entomology 36, 219221.CrossRefGoogle Scholar
Rothschild, A., Schlein, Y. and Ito, S. (1986). A Colour Atlas of Insect Tissues via the Flea, 1st Edn. Wolfe Publishing, London, UK.Google Scholar
Rutledge, L. C., Ward, R. A. and Gould, D. J. (1964). Studies on the feeding response of mosquitoes to nutritive solutions in a new membrane feeder. Mosquito News 24, 407419.Google Scholar
Saleh, F. C., Kirkpatrick, C. E., De Haseth, O. and Lok, J. B. (1988). Occurrence of some blood and intestinal parasites in dogs in Curaçao, Netherlands Antilles. Tropical and Geographical Medicine 40, 318321.Google ScholarPubMed
Viera, C., Villar, E., Cecilian, F. and Simon, F. (2001). The biology and biochemistry of the species. In Heartworm Infection in Humans and Animals (ed. Simon, F. and Genchi, C.), pp. 4344. Universitad de Salamanca, Salamanca, Spain.Google Scholar
Vobis, M., D'Haese, J., Mehlhorn, H. and Mencke, N. (2003). Evidence of horizontal transmission of feline leukemia virus by the cat flea (Ctenocephalides felis). Parasitology Research 91, 467470.CrossRefGoogle ScholarPubMed
Wade, S. and Georgi, J. R. (1988). Survival and reproduction of artificially fed cat fleas, Ctenocephalides felis Bouché (Siphonaptera: Pulicidae). Journal of Medical Entomology 25, 186190.CrossRefGoogle ScholarPubMed
Waladde, S. M., Ochieng, S. A. and Gichuhi, P. M. (1991). Artificial-membrane feeding of the ixodid tick Rhipicephalus appendiculatus to repletion. Experimental and Applied Acarology 11, 297306.CrossRefGoogle ScholarPubMed