Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-11T06:18:47.099Z Has data issue: false hasContentIssue false
  • English
  • Français

Detection of Dirofilaria DNA and host blood-meal identification in Culicoides paolae biting midges

Published online by Cambridge University Press:  31 March 2022

E. Napoli Open the ORCID record for E. Napoli [Opens in a new window] ,
R. Panarese ,
F. La Russa ,
I. Cambera ,
J. A. Mendoza-Roldan ,
D. Otranto Open the ORCID record for D. Otranto [Opens in a new window]  and
E. Brianti Open the ORCID record for E. Brianti [Opens in a new window]
E. Napoli*
Affiliation:
Department of Veterinary Sciences, University of Messina, Messina, Italy
R. Panarese
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy
F. La Russa
Affiliation:
Istituto Zooprofilattico Sperimentale della Sicilia ‘A. Mirri’, Palermo, Italy
I. Cambera
Affiliation:
Department of Veterinary Sciences, University of Messina, Messina, Italy
J. A. Mendoza-Roldan
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy
D. Otranto
Affiliation:
Department of Veterinary Medicine, University of Bari, Valenzano, Italy Faculty of Veterinary Sciences, Bu-Ali Sina University, Hamedan, Iran
E. Brianti
Affiliation:
Department of Veterinary Sciences, University of Messina, Messina, Italy
*
Author for correspondence: E. Napoli, E-mail: enapoli@unime.it
Get access Rights & Permissions [Opens in a new window]

Abstract

The vectorial role of blood-sucking arthropods, other than mosquitoes, has been explored for Dirofilaria immitis and Dirofilaria repens which are filarioids of increasing interest due to their zoonotic potential. Given the expansion of canine heartworm infection in southern Europe due to D. immitis and the report of the infection in Linosa Island (Sicily, Italy), we investigated and focused on the potential involvement of Culicoides spp. in Dirofilaria spp. transmission as well as the blood-meal source in Dirofilaria spp. molecularly positive biting midges. Out of 1791 specimens collected 1773 were morphologically and molecularly identified as Culicoides paolae and 18 as Culicoides obsoletus complex. Of the 1596 females, 4 (0.26%) parous C. paolae tested positive for D. immitis and D. repens (i.e. 2 Culicoides specimens for each filarial species), of which D. immitis-positive samples fed on both humans and dogs and D. repens-positive samples fed only on humans. The detection of D. immitis and D. repens DNA in Culicoides midges suggests their potential involvement in the epidemiology of the filarial nematodes, which may be of medical and veterinary importance in hyper-endemic areas. Findings of this study shed new light on the epidemiology of Dirofilaria spp. infections indicating that further investigations are needed.

Keywords

Biting midgesCulicoides paolaeDirofilaria immitisDirofilaria repensdogsvectors
Type
Research Article
Information
Parasitology , Volume 149 , Issue 7 , June 2022 , pp. 968 - 972
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These two authors contributed equally to this article.

References

Atkinson, CT (1988) Epizootiology of Haemoproteus meleagridis (Protozoa: Haemosporina) in Florida: potential vectors and prevalence in naturally infected Culicoides (Diptera: Ceratopogonidae). Journal of Medical Entomology 25, 39–44.CrossRefGoogle Scholar
Baneth, G, Thamsborg, SM, Otranto, D, Guillot, J, Blaga, R, Deplazes, P and Solano-Gallego, L (2016) Major parasitic zoonoses associated with dogs and cats in Europe. Journal of Comparative Pathology 155, S54–S74.CrossRefGoogle ScholarPubMed
Blanda, V, Blanda, M, La Russa, F, Scimeca, R, Scimeca, S, D'Agostino, R, Auteri, M and Torina, A (2018) Geo-statistical analysis of Culicoides spp. distribution and abundance in Sicily, Italy. Parasites and Vectors 11, 78.CrossRefGoogle ScholarPubMed
Borkent, A (2004) The biting midges, the Ceratopogonidae (Diptera). In Marquardt, W (ed.), Biology of Disease Vectors. Cambridge, UK: Cambridge Academic Press, pp. 113–126.Google Scholar
Bourquia, M, Garros, C, Rakotoarivony, I, Gardès, L, Huber, K, Boukhari, I, Delécolle, JC, Baldet, T, Mignotte, A, Lhor, Y, Khallaayoune, K and Balenghien, T (2019) Update of the species checklist of Culicoides Latreille, 1809 biting midges (Diptera: Ceratopogonidae) of Morocco. Parasites and Vectors 12, 459.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, 530–536.CrossRefGoogle ScholarPubMed
Brianti, E, Panarese, R, Napoli, E, De Benedetto, G, Gaglio, G, Bezerra-Santos, MA, Mendoza-Roldan, JA and Otranto, D (2021) Dirofilaria immitis infection in the Pelagie archipelago: the southernmost hyperendemic focus in Europe. Transboundary and Emerging Diseases, 1–7. doi: 10.1111/tbed.14089Google ScholarPubMed
Cabrera, ED, Carretòn, E, Morchòn, R, Falcòn-Cordòn, Y, Falcòn-Cordòn, S, Simòn, F and Montoya-Alonso, JA (2018) The Canary Islands as a model of risk of pulmonary dirofilariasis in a hyperendemic area. Parasitology Research 117, 933–936.CrossRefGoogle Scholar
Ciuca, L, Simòn, F, Rinaldi, L, Kramer, L, Genchi, M, Cringoli, G, Acatrinei, D, Miron, L and Morchon, R (2018) Seroepidemiological survey of human exposure to Dirofilaria spp. in Romania and Moldova. Acta Tropica 187, 169–174.CrossRefGoogle ScholarPubMed
Dantas-Torres, F and Otranto, D (2020) Overview on Dirofilaria immitis in the Americas, with notes on other filarial worms infecting dogs. Veterinary Parasitology 282, 109–113.CrossRefGoogle ScholarPubMed
Eldridge, BF and Edman, JD (2000) Medical Entomology: A Textbook on Public Health and Veterinary Problems Caused by Arthropods. London: Kluwer Academic.CrossRefGoogle Scholar
Genchi, C and Kramer, LH (2020) The prevalence of Dirofilaria immitis and D. repens in the old world. Veterinary Parasitology 280, 108–995.CrossRefGoogle Scholar
Goffredo, M and Meiswinkel, R (2004) Entomological surveillance of bluetongue in Italy: method of capture, catch analysis and identification of Culicoides biting midges. Veterinaria Italiana 40, 260–265.Google ScholarPubMed
Gonzalez, E, Jiménez, M, Hernández, S, Martín-Martín, I and Molina, R (2017) Phlebotomine sand fly survey in the focus of leishmaniasis in Madrid, Spain (2012–2014): seasonal dynamics, Leishmania infantum infection rates and blood meal preferences. Parasites and Vectors 10, 368.CrossRefGoogle ScholarPubMed
Hakima, B, Hwang, HS and Lee, KY (2020) Molecular identification of Culicoides (Diptera: Ceratopogonidae) species in Algeria. Acta Tropica 202, 105261.CrossRefGoogle ScholarPubMed
Khanzadeh, F, Khaghaninia, S, Maleki-Ravasan, N, Koosha, M and Oshaghi, MA (2020) Molecular detection of Dirofilaria spp. and host blood-meal identification in the Simulium turgaicum complex (Diptera: Simuliidae) in the Aras River Basin, northwestern Iran. Parasites and Vectors 13, 548.CrossRefGoogle ScholarPubMed
Kirkeby, C (2018) Observations of female and mixed sex swarming behaviour in Culicoides Latreille, 1809 (Diptera: Ceratopogonidae). Polish Journal of Entomology 87, 191–197.CrossRefGoogle Scholar
Latrofa, MS, Annoscia, G, Dantas-Torres, F, Traversa, D and Otranto, D (2012) Towards a rapid molecular identification of the common phlebotomine sand flies in the Mediterranean region. Veterinary Parasitology 184, 267–270.CrossRefGoogle ScholarPubMed
Latrofa, MS, Montarsi, F, Ciocchetta, S, Annoscia, G, Dantas-Torres, F, Ravagnan, S, Capelli, G and Otranto, D (2020) Molecular xenomonitoring of Dirofilaria immitis and Dirofilaria repens in mosquitoes from north-eastern Italy by real-time PCR coupled with melting curve analysis. Parasites and Vectors 20, 5–76.Google Scholar
Mellor, PS, Boorman, J and Baylis, M (2000) Culicoides biting midges: their role as arbovirus vectors. Annual Review of Entomology 45, 307–340.CrossRefGoogle ScholarPubMed
Mendoza-Roldan, J, Benelli, G, Panarese, R, Iatta, R, Furlanello, T, Beugnet, F, Zatelli, A and Otranto, D (2020) Leishmania infantum and Dirofilaria immitis infections in Italy, 2009–2019: changing distribution patterns. Parasites and Vectors 13, 193.CrossRefGoogle ScholarPubMed
Mendoza-Roldan, JA, Gabrielli, S, Cascio, A, Manoj, RRS, Bezerra-Santos, MA, Benelli, G, Brianti, E, Latrofa, MS and Otranto, D (2021) Zoonotic Dirofilaria immitis and Dirofilaria repens infection in humans and an integrative approach to the diagnosis. Acta Tropica 223, 106083.CrossRefGoogle Scholar
Napoli, E, Brianti, E, Falsone, L, Gaglio, G, Foit, S, Abramo, F, Annoscia, G, Dantas-Torres, F, Giannetto, S and Otranto, D (2014) Development of Acanthocheilonema reconditum (Spirurida, Onchocercidae) in the cat flea Ctenocephalides felis (Siphonaptera, Pulicidae). Parasitology 141, 1718–1725.CrossRefGoogle Scholar
Nolan, DV, Carpenter, S, Barber, J, Mellor, PS, Dallas, JF, Mordue (Iuntz), AJ and Piertney, SB (2007) Rapid diagnostic PCR assays for members of the Culicoides obsoletus and Culicoides pulicaris species complexes, implicated vectors of bluetongue virus in Europe. Veterinary Microbiology 124, 82–94.CrossRefGoogle ScholarPubMed
Otranto, D, Capelli, G and Genchi, C (2009) Changing distribution patterns of canine vector borne diseases in Italy: leishmaniosis vs dirofilariosis. Parasites and Vectors 2, S2.CrossRefGoogle ScholarPubMed
Otranto, D, Brianti, E, Gaglio, G, Dantas-Torres, F, Azzaro, S and Giannetto, S (2011) Human ocular infection with Dirofilaria repens (Railliet and Henry, 1911) in an area endemic for canine dirofilariasis. American Journal of Tropical Medicine and Hygiene 84, 1002–1004.CrossRefGoogle Scholar
Ozella, L, Cecchetti, M and Pessani, D (2016) Diet of feral cats during the Scopoli's shearwater breeding season on Linosa Island, Mediterranean Sea. Italian Journal of Zoology 83, 589–959.CrossRefGoogle Scholar
Panarese, R, Iatta, R, Latrofa, MS, Zatelli, A, Ćupina, AI, Montarsi, F, Pombi, M, Mendoza-Roldan, JA, Beugnet, F and Otranto, D (2020) Hyperendemic Dirofilaria immitis infection in a sheltered dog population: an expanding threat in the Mediterranean region. International Journal for Parasitology 50, 555–559.CrossRefGoogle Scholar
Rawlings, P (1996) A key, based on wing patterns of biting midges (genus: Culicoides Latreille – Diptera: Ceratopogonidae) in the Iberian Peninsula, for use in epidemiological studies. Graellsia 52, 57–71.CrossRefGoogle Scholar
Sangioni, LA, Horta, MC, Vianna, MCB, Gennari, SM, Soares, RM, Galvão, MAM, Schumaker, TTS, Ferreira, F, Vidotto, O and Labruna, MB (2005) Rickettsial infection in animals and Brazilian spotted fever endemicity. Emerging Infectious Diseases 11, 265–270.CrossRefGoogle ScholarPubMed
Shelley, AJ and Coscaro'n, S (2001) Simuliid blackflies (Diptera: Simuliidae) and ceratopogonid midges (Diptera: Ceratopognidae) as vectors of Mansonella ozzardi (Nematoda: Onchocercidae) in northern Argentina. Memorial of Institute Oswaldo Cruz 96, 451–458.CrossRefGoogle Scholar
Summers, WA (1940) Fleas as acceptable intermediate hosts of the do heartworm, Dirofilaria immitis. Proceedings of the Society for Experimental Biology and Medicine 43, 448–450.CrossRefGoogle Scholar
Ta-Tang, TH, Crainey, JL, Post, RJ, Luz, SL and Rubio, JM (2018) Mansonellosis: current perspectives. Research and Reports in Tropical Medicine 9, 9–24.CrossRefGoogle ScholarPubMed
Veiga, J, Martínez-de la Puente, J, Václav, R, Figuerola, J and Valera, F (2018) Culicoides paolae and C. circumscriptus as potential vectors of avian haemosporidians in an arid ecosystem. Parasites and Vectors 11, 524.CrossRefGoogle Scholar