Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-14T01:26:46.414Z Has data issue: false hasContentIssue false
  • English
  • Français

Prevalence of Dirofilaria repens in dogs living in deltaic coastal plain of the Volturno River (Italy): a geographical risk model of infection

Published online by Cambridge University Press:  23 February 2022

M. Ferrara ,
R. Maglione ,
D. Ciccarelli ,
S.J. Mundis ,
A. Di Loria Open the ORCID record for A. Di Loria [Opens in a new window] ,
M. Pisaroglo de Carvalho  and
D. Santoro
M. Ferrara
Affiliation:
Ambulatorio Veterinario Domitio, Via Veneto 35, 81030Castel Volturno, Italy
R. Maglione
Affiliation:
LABFORVET Laboratorio Analisi Veterinarie, Via Miseno, 80124Napoli, Italy
D. Ciccarelli
Affiliation:
LABFORVET Laboratorio Analisi Veterinarie, Via Miseno, 80124Napoli, Italy
S.J. Mundis
Affiliation:
Department of Geography, University of Florida, Gainesville, FL32608, USA
A. Di Loria*
Affiliation:
Department of Veterinary Medicine and Animal Productions, University Federico II, 80130Napoli, Italy
M. Pisaroglo de Carvalho
Affiliation:
Department of Small Animal Clinical Sciences, University of Florida, Gainesville, FL32608, USA
D. Santoro
Affiliation:
Department of Small Animal Clinical Sciences, University of Florida, Gainesville, FL32608, USA
*
Author for correspondence: A. Di Loria, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The prevalence of vector-associated parasitic infections is high in central-southern Italy. The deltaic coastal plain of the Volturno River has been suspected, by veterinary practitioners, to have a high accidental incidence of Dirofilaria repens. Thus, the goal of this study was to evaluate the prevalence of dirofilariasis and other coinfections frequently described in dogs living in the Volturno area. Blood samples of 100 clinical asymptomatic dogs were examined using a Knott's technique and polymerase chain reaction in order to identify microfilariae. Other vector-borne coinfections were also investigated using ELISA kits. The results were analysed using statistical and Geographic Information System (GIS) software. Microfilariae of D. repens were detected in 10% of the dogs surveyed, with a presence of antibodies against Ehrlichia canis (4/10) and Dirofilaria immitis (1/10). Such high incidence should be considered in light of the zoonotic potential for D. repens and the support for more regular use of repellents to prevent the spread of this disease. The GIS analyses indicated that the study area provides suitable conditions to sustain populations of mosquito vectors and D. repens parasites throughout much of the year.

Keywords

Dirofilaria repensdogprevalencegeographical information systemvector disease
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e12
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.)

References

Agapito, D, Aziz Na, A, Wang, T, Morgan, ER and Wright, I (2018) Subconjunctival Dirofilaria repens infection in a dog resident in the UK. Journal of Small Animal Practice 59, 50–52.CrossRefGoogle Scholar
Attout, T, Martin, C, Babayan, SA, Kozek, WJ, Bazzocchi, C, Oudet, F, Gallagher, IJ, Specht, S and Bain, O (2008) Pleural cellular reaction to the filarial infection Litomosoides sigmodontis is determined by the moulting process, the worm alteration, and the host strain. Parasitology International 57, 201–211.CrossRefGoogle Scholar
Baldi, L, Mizzoni, V and Guarino, A (2004) Canine leishmaniasis in Campania: new and old foci. Parassitologia 46, 217–220.Google ScholarPubMed
Baneth, G, Bourdeau, P, Bourdoiseau, G, et al. (2012) Vector-borne diseases–constant challenge for practicing veterinarians: recommendations from the CVBD world forum. Parasites and Vectors 5, 55.CrossRefGoogle ScholarPubMed
Barlozzari, G, Felice, T, Salvato, L, Conti, R, De Liberato, C, Furzi, F, Gabrielli, S and Scarpulla, M (2021) Usual or unusual presentations of dirofilaria repens in two sibling dogs: a case report. Parasitology Research 120, 109–115.CrossRefGoogle ScholarPubMed
Bazzocchi, C, Genchi, C, Paltrinieri, S, Lecchi, C, Mortarino, M and Bandi, C (2003) Immunological role of the endosymbionts of Dirofilaria immitis: the Wolbachia surface protein activates canine neutrophils with production of IL-8. Veterinary Parasitology 117, 73–83.CrossRefGoogle ScholarPubMed
Brattig, NW, Racz, P, Hoerauf, A and Büttner, DW (2011) Strong expression of TGF-beta in human host tissues around subcutaneous Dirofilaria repens. Parasitology Research 108, 1347–1354.CrossRefGoogle ScholarPubMed
Cancrini, G and Scaglione, F (1984) Osservazioni su due casi di dirofilariasi oculare umana in Sicilia. Parassitologia 26, 273–282.Google Scholar
Cancrini, G, Yanchang, S, Della Torre, A and Coluzzi, M (1988) Influence of temperature on the larval development of Dirofilaria repens in different species of mosquitoes. Parassitologia 30, 38.Google Scholar
Cancrini, G, Romi, R, Gabrielli, S, Toma, L, Di Paolo, M and Scaramozzino, P (2003) First finding of Dirofilaria repens in a natural population of Aedes albopictus. Medical and Veterinary Entomology 17, 448–451.CrossRefGoogle Scholar
Capuano, F, Landolfi, M, Veneziano, V and Cringoli, G (1997) Presenza e diffusione di dirofilaria repens e Dirofilaria immitis in cani della Campania. Atti Società Italiana Scienze Veterinarie 51, 313–314.Google Scholar
Cielecka, D, Zarnowska-Prymek, H, Masny, A, Salamatin, R, Wesołowska, M and Gołąb, E (2012) Human dirofilariosis in Poland: the first cases of autochthonous infections with Dirofilaria repens. Annals of Agricultural and Environmental Medicine 19, 445–450.Google ScholarPubMed
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
Ciuca, L, Vismarra, A, Lebon, W, Beugnet, F, Morchon, R, Rinaldi, L, Cringoli, G, Kramer, L and Genchi, M (2020) New insights into the biology, diagnosis and immune response to Dirofilaria repens in the canine host. Veterinary Parasitology 277, 100029.CrossRefGoogle Scholar
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 102, 243–252.CrossRefGoogle Scholar
Demiaszkiewicz, AW, Karamon, J and Jasik, A (2013) Case of Dirofilaria repens in a testis of a dog. Medycyna Weterynaryjna 69, 124–127.Google Scholar
Farolfi, G, Maseroli, R, Baroni, L and Cauli, F (2009) La rete dinamica nazionale (RDN) ed il nuovo Sistema di riferimento ETRF2000 (Bollettino di Geodesia e Scienze Affini n. 68).Google Scholar
Genchi, C (2018) Dirofilariainfections in Europe: a short update. Proceeding of the 6th European dirofilaria and angiostrongylus days. Parasites and Vectors 11(Suppl 1), 623.Google Scholar
Genchi, C and Kramer, L (2017) Subcutaneous dirofilariosis (Dirofilaria repens): an infection spreading throughout the old world. Parasites and Vectors 10, 1–6.CrossRefGoogle ScholarPubMed
Genchi, C, Kramer, L, Sassera, D and Bandi, C (2012) Wolbachia and its implications for the immunopathology of filariasis. Endocrine Metabolic and Immune Disorders Drug Targets 12, 53–56.CrossRefGoogle ScholarPubMed
Hermosilla, C, Pantchev, N, Dyachenko, V, Gutmann, M and Bauer, C (2006) First autochthonous case of canine ocular Dirofilaria repens infection in Germany. Veterinary Record 158, 134.CrossRefGoogle ScholarPubMed
Hise, AG, Daehnel, K, Gillette-Ferguson, I, et al. (2007) Innate immune responses to endosymbiotic Wolbachia bacteria in Brugia malayi and Onchocerca volvulus are dependent on TLR2, TLR6, myd88, and Mal, but not TLR4, TRIF, or TRAM. Journal of Immunology 178, 1068–1076.CrossRefGoogle ScholarPubMed
Kartashev, V, Batashova, I, Kartashov, S, et al. (2011) Canine and human dirofilariosis in the Rostov region (southern Russia). Veterinary Medicine International 1, 685713.Google Scholar
Lindsay, JR (1965) Identification of canine microfilariae. Journal of American Veterinary Medical Association 146, 1106–1114.Google Scholar
Medlock, JM, Hansford, KM, Schaffner, F, Versteirt, V, Hendrickx, G, Zeller, H and Van Bortel, W (2012) A review of the invasive mosquitoes in Europe: ecology, public health risks, and control options. Vector-Borne and Zoonotic Diseases 12, 435–447.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 & Vectors 13, 193.CrossRefGoogle ScholarPubMed
Mircean, M, Ionică, AM, Mircean, V, Györke, A, Răzvan Codea, A, Tăbăran, FA, Taulescu, M and Dumitrache, MO (2017) Clinical and pathological effects of Dirofilaria repens and Dirofilaria immitis in a dog with a natural co-infection. Parasitology 66, 331–334.CrossRefGoogle Scholar
Omeragić, J, Beck, R, Klarić, D and Bačić, E (2018) Dirofilaria repens in canine testicles in Bosnia and Herzegovina. Veterinaria 67, 37–40.Google Scholar
Otranto, D and Dantas-Torres, F (2010) Canine and feline vector-borne diseases in Italy: current situation and perspectives. Parasites and Vectors 3, 1–12.CrossRefGoogle Scholar
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
Pampiglione, S and Rivasi, F (2000) Human dirofilariasis due to dirofilaria (nochtiella) repens: an update of world literature from 1995 to 2000. Parassitologia 42, 231–254.Google ScholarPubMed
Pampiglione, S, Rivasi, F, Angeli, G, Boldorini, R, Incensati, RM, Pastormerlo, M, Pavesi, M and Ramponi, A (2001) Dirofilariasis due to Dirofilaria repens in Italy, an emergent zoonosis: report of 60 new cases. Histopathology 38, 344–354.CrossRefGoogle ScholarPubMed
Pampiglione, S, Rivasi, F and Gustinelli, A (2009) Dirofilarial human cases in the Old World, attributed to Dirofilaria immitis: a critical analysis. Histopathology 54, 192–204.CrossRefGoogle ScholarPubMed
Pantchev, N, Etzold, M, Daugschies, A and Dyachenko, V (2011) Diagnosis of imported canine filarial infections in Germany 2008–2010. Parasitology Research 109, 61–76.CrossRefGoogle ScholarPubMed
Petry, G, Genchi, M, Schmidt, H, Schaper, R, Lawrenz, B and Genchi, C (2015) Evaluation of the adulticidal efficacy of imidacloprid 10%/moxidectin 2.5%(w/v) spot-on (advocate®, advantage® multi) against Dirofilaria repens in experimentally infected dogs. Parasitology Research 114, 131–144.CrossRefGoogle Scholar
Pietikäinen, R, Nordling, S, Jokiranta, S, et al. (2017) Dirofilaria repens transmission in southeastern Finland. Parasites and Vectors 10, 1–6.CrossRefGoogle ScholarPubMed
Pingen, CH, Lorentz, S, Magnis, J, Menn, B, Schaper, R and Naucke, TJ (2009) Successful treatment of Dirofilaria repens infections in dogs with melarsomine (immiticide, merial), against adults and a combination of moxidectin 2.5%/imidacloprid 10% (advocate, Bayer) against microfilaria. pp. 146–147 in Proceedings of the 8th International Conference of the World Association for the Advancement of Veterinary Parasitology (WAAP’09). August 2009; Alberta, Canada.Google Scholar
Puccini, V and Abbenante, MG (1980) Dirofilariosi del cane in Puglia: indagine epizoologica. Atti Società Italiana Scienze Veterinarie 34, 323.Google Scholar
Ravindran, R, Julie, B, Swapna, SA, Jerin, F, Lenka, D, Nandakumar, S and Sabu, SM (2016) Research note Dirofilaria repens in scrotum of dogs. Tropical Biomedicine 33, 842–846.Google Scholar
Romi, R, Severini, F and Toma, L (2006) Cold acclimation and overwintering of female Aedes albopictus in Roma. Journal of American Mosquitos Control Association 22, 149–151.CrossRefGoogle ScholarPubMed
Rossi, E, Rinaldi, L, Musella, V, Veneziano, V, Carbone, S, Gradoni, L, Cringoli, G and Maroli, M (2007) Mapping the main Leishmania phlebotomine vector in the endemic focus of the Mt. Vesuvius in southern Italy. Geospatial Health 1, 191–198.CrossRefGoogle Scholar
Ruberti, D and Vigliotti, M (2017) Land use and landscape pattern changes driven by land reclamation in a coastal area: the case of Volturno delta plain, Campania region, southern Italy. Environmental Earth Science 76, 1–19.Google Scholar
Sabūnas, V, Radzijevskaja, J, Sakalauskas, P, Petkevicius, S, Karveliene, B, Ziliukiene, J, Lipatova, I and Paulauskas, A (2019) Dirofilaria repens in dogs and humans in Lithuania. Parasites and Vectors 12, 1–10.CrossRefGoogle ScholarPubMed
Simón, F, Siles-Lucas, M, Morchón, R, Gonzàlez-Miguel, J, Mellado, I, Carretòn, E and Montoya-Alonso, JA (2012) Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clinical Microbiology Reviews 25, 507–544.CrossRefGoogle ScholarPubMed
Sloss, MW, Kemp, RL and Zayac, AM (1994) Veterinary clinical parasitology. Ames, USA, Iowa State University Press.Google Scholar
Solano-Gallego, L, Trotta, M, Razia, L, Furlanello, T and Caldin, M (2006) Molecular survey of Ehrlichia canis and Anaplasma phagocytophilum from blood of dogs in Italy. Annals of the New York Academy of Sciences 1078, 515–518.CrossRefGoogle ScholarPubMed
Tarello, W (2002) Cutaneous lesions in dogs with dirofilaria (nochtiella) repens infestation and concurrent tick-borne transmitted diseases. Veterinary Dermatology 13, 267–274.CrossRefGoogle ScholarPubMed
Traversa, D, Aste, G, Milillo, P, Capelli, G, Pampurini, F, Tunesi, C, Santori, D, Paoletti, B and Boari, A (2010) Autochthonous foci of canine and feline infections by Dirofilaria immitis and Dirofilaria repens in central Italy. Veterinary Parasitology 169, 128–132.CrossRefGoogle ScholarPubMed
Wan, Z (2007) Collection-5 MODIS land surface temperature products users’ guide. ICESS. Santa Barbara, University of California.Google Scholar
Webber, WA and Hawking, F (1955) Experimental maintenance of Dirofilaria repens and D. immitis in dogs. Experimental Parasitology 4(2), 143–164.CrossRefGoogle Scholar