Skip to main content
SpringerLink
Log in

Current surveys on the prevalence and distribution of Dirofilaria spp. and Acanthocheilonema reconditum infections in dogs in Romania

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

During the last decades, Dirofilaria spp. infection in European dogs has rapidly spread from historically endemic areas towards eastern and northeastern countries, but little or no information is available from these geographical regions. The present study provides a picture of filarial infections in dogs from Romania and compares two tests for the diagnosis of Dirofilaria immitis. From July 2010 to March 2011, blood samples were collected from 390 dogs from nine counties of Romania and serological SNAP tests were performed for the detection of D. immitis antigen. The remaining blood clots were subsequently used for DNA extraction followed by multiplex PCR for assessing filarioid species diversity (i.e. D. immitis, Dirofilaria repens and Acanthocheilonema reconditum). Based on molecular detection, an overall prevalence of 6.92 % (n = 27; 95 % confidence interval (CI) 4.70–10.03 %) for D. repens, 6.15 % (n = 24; 95 % CI 4.07–9.14 %) for D. immitis and 2.05 % (n = 8; 95 % CI 0.96–4.16 %) for A. reconditum was recorded, with significant variations according to sampling areas. Coinfections of D. immitis and D. repens were recorded in 23.91 % (n = 11) positive dogs. A slightly higher prevalence for D. immitis was detected at the SNAP test (n = 28, 7.17 %; 95 % CI 4.91–10.33 %), but this difference was not statistically significant (p = 0.66). However, only 53.57 % (n = 15) of antigen-positive dogs were confirmed by PCR, while other dogs (n = 9) PCR positive for D. immitis were negative at the serology. The present study shows that Dirofilaria species are endemic in the southern and southeastern areas of Romania, This article also provides, for the first time, an epidemiological picture of the distribution of A. reconditum in Romania.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abraham D (1988) Biology of Dirofilaria immitis. In: Boreham PFL, Atwell RB (eds) Dirofilariasis. CRC Press, London, pp 29–46

    Google Scholar 

  • Albanese F, Abramo F, Braglia C, Caporali C, Venco L, Vercelli A, Ghibaudo G, Leone F, Carrani F, Giannelli A, Otranto D (2013) Nodular lesions due to infestation by Dirofilaria repens in dogs from Italy. Vet Dermatol 24:255–256. doi:10.1111/vde.12009

    Article  PubMed  Google Scholar 

  • Albrechtová K, Sedlák K, Petrželková KJ, Hlaváč J, Mihalca AD, Lesingirian A, Kanyari PWN, Modrý D (2011) Occurrence of filaria in domestic dogs of Samburu pastoralists in Northern Kenya and its associations with canine distemper. Vet Parasitol 182:230–238. doi:10.1016/j.vetpar.2011.05.042

    Article  PubMed  Google Scholar 

  • American Heartworm Society (2014) Current canine guidelines for the prevention, diagnosis and management of heartworm (Dirofilaria immitis) infection in dogs. www.heartwormsociety.org (consulted June 2014)

  • Aoki Y, Yasunori F, Tada I (2011) Basic studies on filaria and filariasis. Trop Med Health 39:51–55. doi:10.2149/tmh.39-1-suppl_2-51

    PubMed Central  PubMed  Google Scholar 

  • Bocková E, Rudolf I, Kočišová A, Betášová L, Venclíková K, Mendel J, Hubálek Z (2013) Dirofilaria repens microfilariae in Aedes vexans mosquitoes in Slovakia. Parasitol Res 112:3465–3470. doi:10.1007/s00436-013-3526-9

    Article  PubMed Central  PubMed  Google Scholar 

  • Brianti E, Gaglio G, Napoli E, Giannetto S, Dantas-Torres F, Bain O, Otranto D (2012) New insights into the ecology and biology of Acanthocheilonema reconditum (Grassi, 1889) causing canine subcutaneous filariosis. Parasitology 139:530–536. doi:10.1017/S0031182011002198

    Article  PubMed  Google Scholar 

  • Chandrashekar R, Mainville CA, Beall MJ, O’Connor T, Eberts MD, Alleman AR, Gaunt SD, Breitschwerdt EB (2010) Performance of a commercially available in-clinic ELISA for the detection of antibodies against Anaplasma phagocytophilum, Ehrlichia canis, and Borrelia burgdorferi and Dirofilaria immitis antigen in dogs. Am J Vet Res 71:1443–1450. doi:10.2460/ajvr.71.12.1443

    Article  PubMed  Google Scholar 

  • Ciocan R, Darăbuș G, Jascó O, Fok É (2010) Detection of Dirofilaria spp. in dogs by PCR. USAMV Bull 67:40–44

    Google Scholar 

  • Ciocan R, Mederle N, Jacsó O, Tánczos B, Fok É (2013) Autochthonous cases of Dirofilaria in dogs from Timiş County (Western Part) Romania. Global Journal of Medical Research XIII: 29-34

  • Courtney CH, Zeng QY (2001) Comparison of heartworm antigen test kit performance in dogs having low heartworm burdens. Vet Parasitol 96:317–322

    Article  PubMed  CAS  Google Scholar 

  • Demiaszkiewicz AW, Polańczyk G, Osińska B, Pyziel AM, Kuligowska I, Lachowicz J, Sikorski A (2014) Prevalence and distribution of Dirofilaria repens Railliet et Henry, 1911 in dogs in Poland. Pol J Vet Sci 17:515–517

    PubMed  CAS  Google Scholar 

  • Di Cesare A, Otranto D, Di Giulio E, Simonato G, Latrofa MS, La Torre F, Coccia G, Traversa D (2013) Microfilarial periodicity of Dirofilaria repens in naturally infested dogs. Parasitol Res 112:4273–4279. doi:10.1007/s00436-013-3619-5

    Article  PubMed  Google Scholar 

  • Dobesová R, Svobodová Z, Svobodová V (2007) Dirofilariosis in dogs - the actual situation in the Czech Republic. In Genchi C, Rinaldi L, Cringoli G (eds), Mappe Parassitologiche 8 - Dirofilaria immitis and D. repens in dog and cat and human infections. Rolando Editore, Naples, p. 198

  • Fok É, Kiss G, Majoros G, Jacsó O, Farkas R, Gyurkovszky M (2007) Preliminary results of an epidemiological survey on dirofilariosis of dogs and cats in Hungary. In Genchi C, Rinaldi L, Cringoli G (eds), Mappe Parassitologiche 8 - Dirofilaria immitis and D. repens in dog and cat and human infections. Rolando Editore, Naples, pp. 195-196

  • Genchi C, Solari Basano F, Bandi C, Di Sacco B, Venco L, Vezzoni A, Cancrini G (1995) Factors influencing the spread of heartworms in Italy: interaction between Dirofilaria immitis and Dirofilaria repens. In: Proceedings of Heartworm Symposium ’95. American Heartworm Society, Batavia, Illinois, pp. 65-71

  • Genchi C, Venco L, Genchi M (2007) Guideline for the laboratory diagnosis of canine and feline Dirofilaria infections. In Genchi C, Rinaldi L, Cringoli G (eds), Mappe Parassitologiche 8 - Dirofilaria immitis and D. repens in dog and cat and human infections. Rolando Editore, Naples, pp. 138-144

  • Genchi C, Rinaldi L, Mortarino M, Genchi M, Cringoli G (2009) Climate and Dirofilaria infection in Europe. Vet Parasitol 163:286–292. doi:10.1016/j.vetpar.2009.03.026

    Article  PubMed  Google Scholar 

  • Genchi C, Mortarino M, Rinaldi L, Cringoli G, Traldi G, Genchi M (2011) Changing climate and changing vector-borne disease distribution: the example of Dirofilaria in Europe. Vet Parasitol 176:295–299. doi:10.1016/j.vetpar.2011.01.012

    Article  PubMed  Google Scholar 

  • Hamel D, Silaghi C, Lescai D, Pfister K (2012) Epidemiological aspects on vector-borne infections in stray and pet dogs from Romania and Hungary with focus on Babesia spp. Parasitol Res 110:1537–1545. doi:10.1007/s00436-011-2659-y

    Article  PubMed  Google Scholar 

  • Hamel D, Silaghi C, Zapadynska S, Kudrin A, Pfister K (2013) Vector-borne pathogens in ticks and EDTA-blood samples collected from client-owned dogs, Kiev, Ukraine. Ticks Tick-Borne Dis 4:152–155. doi:10.1016/j.ttbdis.2012.08.005

    Article  PubMed  Google Scholar 

  • Hawking F (1956) The periodicity of microfilariae. IV. Stimuli affecting the migration of the microfilariae of Dirofilaria aethiops, D. immitis, D. repens, Dipetalonema blanci and Litomosoides carinii. Trans R Soc Trop Med Hyg 50:397–417

    Article  PubMed  CAS  Google Scholar 

  • Hermosilla C, Pantchev N, Dyachenko V, Gutmann M, Bauer C (2006) First autochthonous case of canine ocular Dirofilaria repens infection in Germany. Vet Rec 158:134–135

    Article  PubMed  CAS  Google Scholar 

  • Ionică AM, D’Amico G, Mitková B, Kalmár Z, Annoscia G, Otranto D, Modrý D, Mihalca AD (2014) First report of Cercopithifilaria spp. in Eastern Europe with an overview of their geographic distribution in Europe. Parasitol Res 113:2761–2764. doi:10.1007/s00436-014-3931-8

    Article  PubMed  Google Scholar 

  • Krämer F, Schaper R, Schunack B, Połozowski A, Piekarska J, Szwedko A, Jodies R, Kowalska D, Schüpbach D, Pantchev N (2014) Serological detection of Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis antibodies and Dirofilaria immitis antigen in a countrywide survey in dogs in Poland. Parasitol Res 113:3229–3239. doi:10.1007/s00436-014-3985-7

    Article  PubMed Central  PubMed  Google Scholar 

  • Kronefeld M, Kampen H, Sassnau R, Werner D (2014) Molecular detection of Dirofilaria immitis, Dirofilaria repens and Setaria tundra in mosquitoes from Germany. Parasit Vectors 16:7–30. doi:10.1186/1756-3305-7-30

    Google Scholar 

  • Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  PubMed  CAS  Google Scholar 

  • Latrofa MS, Weigl S, Dantas-Torres F, Annoscia G, Traversa D, Brianti E, Otranto D (2012) A multiplex PCR for the simultaneous detection of species of filarioids infesting dogs. Acta Trop 122:150–154. doi:10.1016/j.actatropica.2012.01.006

    Article  PubMed  CAS  Google Scholar 

  • Little SE, Munzing C, Heise SR, Allen KE, Starkey LA, Johnson EM, Meinkoth J, Reichard MV (2014) Pre-treatment with heat facilitates detection of antigen of Dirofilaria immitis in canine samples. Vet Parasitol 203:250–252. doi:10.1016/j.vetpar.2014.01.007

    Article  PubMed  CAS  Google Scholar 

  • Maslov DA, Lukeš J, Jirků M, Simpson A (1996) Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. Mol Biochem Parasitol 75:197–205. doi:10.1016/0166-6851(95)02526-X

    Article  PubMed  CAS  Google Scholar 

  • Masny A, Lewin T, Salamatin R, Golab E (2011) Autochthonous canine Dirofilaria repens in the vicinity of Warsaw. Pol J Vet Sci 14:659–661. doi:10.2478/v10181-011-0098-4

    PubMed  CAS  Google Scholar 

  • Mircean V, Dumitrache MO, Györke A, Pantchev N, Jodies R, Mihalca AD, Cozma V (2012) Seroprevalence and geographic distribution of Dirofilaria immitis and and tick-borne infections (Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis) in dogs from Romania. Vector-borne and Zoonotic Dis 12:595–604. doi:10.1089/vbz.2011.0915

    Article  Google Scholar 

  • Miterpáková M, Antolová D, Hurníková Z, Dubinský P, Pavlacka A, Németh J (2010) Dirofilaria infections in working dogs in Slovakia. J Helminthol 84:173–176. doi:10.1017/S0022149X09990496

    Article  PubMed  Google Scholar 

  • Morgan ER, Jefferies R, Krajewski M, Ward P, Shaw SE (2009) Canine pulmonary angiostrongylosis: the influence of climate on parasite distribution. Parasitol Int 58:406–410. doi:10.1016/j.parint.2009.08.003

    Article  PubMed  Google Scholar 

  • Nelson GS (1962) Dipetalonema reconditum (Grassi, 1889) from the dog with a note on its development in the flea, Ctenocephalides felis and the louse, Heterodoxus spiniger. J Helminthol 36:297–308

    Article  Google Scholar 

  • Nelson CT, McCall JW, Rubin SB, Buzhardt LF, Dorion DW, Graham W, Longhofer SL, Guerrero J, Robertson-Plouch C, Paul A (2005) Guidelines for the diagnosis, prevention and management of heartworm (Dirofilaria immitis) infection in dogs. Vet Parasitol 133:255–266

    Article  PubMed  Google Scholar 

  • Nicolescu G, Vladimirescu A, Ciolpan O (2003) The distribution of mosquitoes in Romania (Diptera: Culicidae). Part III: Detailed maps for Anopheles, Aedes and Culex. Eur Mosquito Bull 14:25–31

    Google Scholar 

  • Orihel T, Eberhard ML (1998) Zoonotic filariasis. Clin Microbiol Rev 11:366–381

    PubMed Central  PubMed  CAS  Google Scholar 

  • Otranto D, Dantas-Torres F, Brianti E, Traversa D, Petrić D, Genchi C, Capelli G (2013) Vector-borne helminths of dogs and humans in Europe. Parasit Vectors 6:16. doi:10.1186/1756-3305-6-16

    Article  PubMed Central  PubMed  Google Scholar 

  • Pampiglione S, Rivasi F (2000) Human dirofilariasis due to Dirofilaria (Nochtiella) repens: an update of world literature from 1995 to 2000. Parassitologia 42:231–254

    PubMed  CAS  Google Scholar 

  • Pantchev N, Schaper R, Limousin S, Norden N, Weise M, Lorentzen L (2009a) Occurrence of Dirofilaria immitis and tick-borne infections caused by Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and Ehrlichia canis in domestic dogs in France: results of a countrywide serologic survey. Parasitol Res 105(Suppl 1):S101–S113. doi:10.1007/s00436-009-1501-2

    Article  PubMed  Google Scholar 

  • Pantchev N, Norden N, Lorentzen L, Rossi M, Rossi U, Brand B, Dyachenko V (2009b) Current surveys on the prevalence and distribution of Dirofilaria spp. in dogs in Germany. Parasitol Res 105(Suppl 1):S63–S74. doi:10.1007/s00436-009-1497-7

    Article  PubMed  Google Scholar 

  • Pantchev N, Etzold M, Daugschies A, Dyachenko (2011) Diagnosis of imported canine filarial infections in Germany 2008-2010. Parasitol Res 109:S61–S76. doi:10.1007/s00436-011-2403-7

    Article  PubMed  Google Scholar 

  • Paşca S, Miron L, Acatrinei D, Mihalachi S (2008) Both cardio-vasculary and subcutaneous forms of dirofilariosis in dog: a case report. In: Miron L, Mareş M (Eds) Scientific Papers Veterinary Medicine Iaș i, vol. 51, pp. 123-127

  • Popesco F (1933) Des foyers de filariose canine en Roumanie. Arh Vet 5–6:145–148

    Google Scholar 

  • Popesco F (1935) Contribution a l’étude hématologique et au traitement de la filariose canine. Arch Roum Pathol Exp 2:215–261

    Google Scholar 

  • Popovici TA (1916) La filariose chez le chien, recherches cliniques et experimentales. Arh Vet 13:33–34

    Google Scholar 

  • Rawlings CA, Dawe DL, McCall JW, Keith JC, Prestwood AK (1982) Four types of occult Dirofilaria immitis infection in dogs. J Am Vet Med Assoc 180:1323–1326

    PubMed  CAS  Google Scholar 

  • Sapierzyński R, Fabisiak M, Sałamaszyńska A (2010) Several cases of dirofilariosis accidentally diagnosed in dogs from Poland, including two PCR positive Dirofilaria repens cases. Pol J Vet Sci 13:545–547

    PubMed  Google Scholar 

  • Sassnau R, Genchi C (2013) Qualitative risk assessment for the endemisation of Dirofilaria repens in the state of Brandenburg (Germany) based on temperature-dependent vector competence. Parsitol Res 112:2647–2652. doi:10.1007/s00436-013-3431-2

    Article  CAS  Google Scholar 

  • Schnyder M, Deplazes P (2012) Cross-reactions of sera from dogs infected with Angiostrongylus vasorum in commercially available Dirofilaria immitis test kits. Parasit Vectors 5:258. doi:10.1186/1756-3305-5-258

    Article  PubMed Central  PubMed  Google Scholar 

  • Schnyder M, Stebler K, Naucke TJ, Lorentz S, Deplazes P (2014) Evaluation of a rapid device for serological in-clinic diagnosis of canine angiostrongylosis. Parasit Vectors 7:72. doi:10.1186/1756-3305-7-72

    Article  PubMed Central  PubMed  Google Scholar 

  • Sergeant, ESG (2014) Epitools epidemiological calculators. Aus Vet Animal Health Services and Australian Biosecurity Cooperative Research Centre for Emerging Infectious Disease. Available at: http://epitools.ausvet.com.au

  • Silbermayr K, Eigner B, Joachim A, Duscher GG, Seidel B, Allerberger F, Indra A, Hufnagl P, Fuehrer HP (2014) Autochthonous Dirofilaria repens in Austria. Parasit Vectors 7:226. doi:10.1186/1756-3305-7-226

    Article  PubMed Central  PubMed  Google Scholar 

  • Svobodová Z, Svobodová V, Genchi C, Forejtek P (2006) The first report of authochthonous dirofilariosis in dogs in the Czech Republic. Helminthologia 43:242–245. doi:10.2478/s11687-006-0046-5

  • Świątalska A, Demiaszkiewicz AW (2012) First autochthonous case of Dirofilaria immitis invasion in dog in Poland. Życie Weterynaryjne 87:685–686

    Google Scholar 

  • Tolnai Z, Széll Z, Sproch Á, Szeredi L, Sréter T (2014) Dirofilaria immitis: an emerging parasite in dogs, red foxes and golden jackals in Hungary. Vet Parasitol 203:339–342. doi:10.1016/j.vetpar.2014.04.004

    Article  PubMed  CAS  Google Scholar 

  • Tudor P, Mateescu R, Tudor N (2013) Dirofilaria infection in dogs from Târgovişte area, Romania. Current Opinion in Biotechnology 24 Supplement1: S51-S52. doi: 10.1016/j.copbio.2013.05.123

  • Velasquez L, Blagburn BL, Duncan-Decoq R, Johnson EM, Allen KE, Meinkoth J, Gruntmeir J, Little SE (2014) Increased prevalence of Dirofilaria immitis antigen in canine samples after heat treatment. Vet Parasitol, 206:67–70. doi: 10.1016/j.vetpar.2014.03.021

  • Venco L (2007) Heartworm (Dirofilaria immitis) disease in dogs. In Genchi C, Rinaldi L, Cringoli G (eds), Mappe Parassitologiche 8 - Dirofilaria immitis and D. repens in dog and cat and human infections. Rolando Editore, Naples, pp. 117-125

  • Weil GJ (1987) Dirofilaria immitis: identification and partial characterization of parasite antigens in the serum of infected dogs. Exp Parasitol 64:244–251

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The research was financed from grant PCE 236/2011. The work was done under the frame of EurNegVec COST Action TD1303. Dr. Mirabela Dumitrache’s work was financed by POSDRU grant no. 159/1.5/S/136893, grant with title “Parteneriat strategic pentru creşterea calităţii cercetării ştiinţifice din universităţile medicale prin acordarea de burse doctorale şi postdoctorale – DocMed.Net_2.0. We are indebted to local veterinary personnel and regional veterinary authorities as well to the Danube Delta Biosphere Reserve for issuing research permits. We also wish to express our gratitude to Martina Gallusová, Moneeb Qablan and Stefania Latrofa.

Conflict of interest

There are no commercial associations for author N.P. of IDEXX Laboratories; there is no commercial conflict of interest since the information generated here is solely for scientific dissemination. There are no conflicts of interest to report by any author.

Author information

Authors and Affiliations

  1. Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, Calea Mănăştur 3-5, 400372, Cluj-Napoca, Romania

    Angela Monica Ionică, Ioana Adriana Matei, Viorica Mircean, Mirabela Oana Dumitrache, Gianluca D’Amico, Adriana Győrke & Andrei Daniel Mihalca

  2. IDEXX Laboratories, 71636, Ludwigsburg, Germany

    Nikola Pantchev

  3. Dipartimento di Medicina Veterinaria, Università degli Studi di Bari, Str. prov. per Casamassima km 3, 70010, Valenzano, Bari, Italy

    Giada Annoscia & Domenico Otranto

  4. Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, 612 42, Brno, Czech Republic

    Kateřina Albrechtová & David Modrý

  5. CEITEC –VFU, University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1/3, 612 42, Brno, Czech Republic

    David Modrý

  6. Institute of Parasitology, Biology Centre of Academy of Sciences of the Czech Republic, v.v.i., České Budějovice, Czech Republic

    David Modrý

Authors
  1. Angela Monica Ionică
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ioana Adriana Matei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Viorica Mircean
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mirabela Oana Dumitrache
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gianluca D’Amico
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Adriana Győrke
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nikola Pantchev
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Giada Annoscia
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kateřina Albrechtová
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Domenico Otranto
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. David Modrý
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Andrei Daniel Mihalca
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angela Monica Ionică.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ionică, A.M., Matei, I.A., Mircean, V. et al. Current surveys on the prevalence and distribution of Dirofilaria spp. and Acanthocheilonema reconditum infections in dogs in Romania. Parasitol Res 114, 975–982 (2015). https://doi.org/10.1007/s00436-014-4263-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4263-4

Keywords

Search

Navigation