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Diagnosis of Imported Canine Filarial Infections in Germany 2008 – 2010

Abstract

Filarial infections of dogs are attracting attention across Europe because of the risk of spread into previously non-endemic areas (e.g. Dirofilaria repens with Culicidae as vectors) and as emerging zoonotic agents. The occurrence of filarial infections in German dogs has been analysed based on 8,545 samples collected either from imported animals or following travel into endemic regions. All samples were tested by means of modified Knott’s test and heartworm antigen assay within the period 2008 – 2010. Heartworm antigen was detected in 127 samples (1.49 %; 95 % CI: 1.25 – 1.77 %), but only 38 dogs also had microfilariae in their blood samples. On the other hand, 125 animals (1.46 %; 95 % CI: 1.23 – 1.74 %) were only positive in the Knott’s test. For discrimination by means of PCR and sequencing a total of 73 blood samples as well as two samples of adult worms were included, which have been sent by veterinarians during 2008 – 2010. A mono-infection caused by D. repens was detected in 35 cases, while D. immitis was proven in 15 samples, with 6 of these showing a combination of D. immitis and D. repens. Imported Dipetalonema dracunculoides (transmitted by Rhipicephalus sanguineus or Hippobosca longipennis) or Acanthocheilonema reconditum (fleas and lice serve as intermediate hosts) infections were diagnosed in 24 cases and in a single sample a co-infection of A. reconditum and D. repens was evident. D. repens was the most common filarial infection imported and it was introduced into Germany from eleven European countries. Slovenia and Hungary are reported for the first time as endemic for D. repens and A. reconditum, respectively. Furthermore this study reports, to the best of our knowledge, for the first time import of D. dracunculoides from the Canary Islands, A. reconditum from Majorca, D. immitis from Corfu and a co-infection of D. repens and A. reconditum from Spain as well as mixed infections of D. repens and D. immitis from Corfu, Sardinia and Bulgaria. Co-infections with other arthropod-borne infections as well as therapeutical follow-up were also considered. Selamectin (as spot-on formulation) was not able to clear microfilaraemia in dogs infected with either D. repens, A. reconditum or D. dracunculoides, whereas a topical moxidectin/imidacloprid formulation was able to eliminate microfilariae in one dog infected with A. reconditum.

References

  • Anderson RC (2000) Nematodes parasites of vertebrates, their development and transmission, 2nd edn. CABI Publishing, New York, p 650.

    Book  Google Scholar 

  • Brglez J, Senk L (1987) Dirofilaria immitis (Leidy, 1856) Raillet et Henry, 1911, pri psu. Veterinarstvo 24:69 – 72.

    Google Scholar 

  • Cancrini G, Scaramozzino P, Gabrielli S, Di Paolo M, Toma L, Romi R (2007) Aedes albopictus and Culex pipiens implicated as natural vectors of Dirofilaria repens in Central Italy. J Med Entomol 44:1064 – 1066.

    PubMed  Article  CAS  Google Scholar 

  • Carret C, Walas F, Carcy B, Grande N, Precigout E, Moubri K, Schetters TP, Gorenflot A (1999) Babesia canis canis, Babesia canis vogeli, Babesia canis rossi: differentiation of the three subspecies by a restriction fragment length polymorphism analysis on amplified small subunit ribosomal RNA genes. J Eukaryot Microbiol 46:298 – 303.

    PubMed  Article  CAS  Google Scholar 

  • Cazelles C, Montagner C (1995) Deux cas de dirofilariose cutanée associée à une leishmaniose. Point Vét 27:71 – 73.

    Google Scholar 

  • Chauve CM (1997) Importance in France of the infestation by Dirofilaria (Nochtiella) repens in dogs. Parassitologia 39:393 – 395.

    PubMed  CAS  Google Scholar 

  • Courtney CH, Zeng QY (2001a) Relationship between microfilaria count and sensitivity of the direct smear for diagnosis of canine dirofilariosis. Vet Parasitol 94(3):199 – 204.

    PubMed  Article  CAS  Google Scholar 

  • Courtney CH, Zeng QY (2001b) Comparison of heartworm antigen test kit performance in dogs having low heartworm burdens. Vet Parasitol 96(4):317 – 322.

    PubMed  Article  CAS  Google Scholar 

  • Demiaszkiewicz AW, Polanczyk G (2010) The first case of Dirofilaria repens invasion in a dog in Poland. Mag Weter 154:254 – 256.

    Google Scholar 

  • Ducos De Lahitte J (1990) Épidémiologie des filarioses en France. Prat Méd Chir Anim Comp 25(Suppl 3)(Numéro spécial: Dirofilariose canine):305 – 310.

  • Duscher G, Feiler A, Wille-Piazzai W, Bakonyi T, Leschnik M, Miterpakova M, Kolodziejek J, Nowotny N, Joachim A (2009) Detection of Dirofilaria in Austrian dogs. Berl Münch Tierärztl Wochenschr 122:199 – 203.

    PubMed  Google Scholar 

  • Džaja P, Beck A, Kiš G, Gudan Kurilj A, Živičnjak T, Artuković B, Beck R, Hohšteter M, Zuckermann Šoštarić IC, Grabarević Z (2008) Dirofilaria repens infection in a dog in Croatia – a case report. Veterinarski Arhiv 78(6):521 – 527.

    Google Scholar 

  • Eckert J, Friedhoff KT, Zahner H, Deplazes P (2008) Lehrbuch der Parasitologie für die Tiermedizin. Enke Verlag, Stuttgart, p 632.

    Google Scholar 

  • Farnell DR, Faulkner DR (1978) Prepatent period of Dipetalonema reconditum in experimentally-infected dogs. J Parasitol 64(3):565 – 567.

    PubMed  Article  CAS  Google Scholar 

  • Favia G, Lanfrancotti A, Della TA, Cancrini G, Coluzzi M (1996) Polymerase chain reaction-identification of Dirofilaria repens and Dirofilaria immitis. Parasitology 113(Pt 6): 567 – 571.

    PubMed  Article  Google Scholar 

  • Fok E, Jacsó O, Szebeni Z, Gyorffy A, Sükösd L, Lukács Z, Schaper R (2010) Elimination of Dirofilaria (syn. Nochtiella) repens microfilariae in dogs with monthly treatments of moxidectin 2.5 %/imidacloprid 10 % (Advocate, Bayer) spot-on. Parasitol Res 106(5):1141 – 1149.

    PubMed  Article  Google Scholar 

  • Genchi C, Rinaldi L, Mortarino M, Genchi M, Cringoli G (2008) Climate and Dirofilaria infection in Europe. Vet Parasitol. doi:10.1016/j. vetpar. 2009.03.026.

  • Genchi C, Mortarino M, Genchi M, Rinaldi L (2009) The spreading of Dirofilaria infections in the European countries. In: Morchón R, Simón F, Montoya JA, Genchi C (eds) Second European Dirofilaria Days 2009, Salamanca, Spain, pp 54 – 67.

    Google Scholar 

  • Georgieva D, Kirkova Z, Ivanov A (2001) A study on the incidence and diagnostics of dirofilariosis (heartworm disease) in carnivores. Bulg J Vet Med 4(4):231 – 236.

    Google Scholar 

  • Gomez-Bautista M, Rojo-Vazquez FA (1990) Dirofilariosis canina y humana en España. Med Vet 7:71 – 74.

    Google Scholar 

  • Globokar M, Pantchev N, Zahner H, Bauer C (2010) Von Arthropoden übertragene Erreger bei Hunden mit Import- oder Reise-Anamnese oder mit Verdachtsdiagnose – Nachweishäufigkeit in Deutschland (2004 – 2006). DVG-Tagung Fachgruppe Parasitologie „Parasitologie und Parasitenbekämpfung: Neues und Neue Wege“ München, 07.–09.07.2010, Tierärztl Prax Ausg G Grosstiere Nutztiere 4:A19.

  • Guerrero J, Rojo F, Rodenas A (1989) Estudio de la incidencia de la enfermedad del gusano del corazón en la población canina española. Med Vet 6:217 – 220.

    Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Hirsch M, Pantchev N (2008) Vorkommenshäufigkeit der Reisekrankheiten Leishmaniose, Ehrlichiose, Babesiose und Dirofilariose bei in Deutschland lebenden Hunden. Kleintierpraxis 53(Heft 3):154 – 165.

    Google Scholar 

  • Jacsó O, Mándoki M, Majoros G, Pétsch M, Mortarino M, Genchi C, Fok E (2009) Dirofilaria immitis (Leidy, 1856) infection in a dog, first autochthonous case in Hungary. In: Morchón R, Simón F, Montoya JA, Genchi C (eds) Second European Dirofilaria Days 2009, Salamanca, Spain, p 223.

    Google Scholar 

  • Jacsó O, Fok E, Kiss G, Kökeny G, Lang Z (2010) Preliminary findings on the efficacy of selamectin in the treatment of dogs naturally infected with Dirofilaria repens. Acta Vet Hung 58(4):405 – 412.

    PubMed  Article  Google Scholar 

  • Kanev I, Kamenov I, Ganchev G, Prelezov P, Tzvetkov Y, Toucheva V, Halacheva M, Georgieva D, Vuchev D, Tanchev T, Slavova G (1996) Dirofilaria repens and Dirofilaria immitis in animals and humans in Bulgaria. Parassitologia 38:358.

    Google Scholar 

  • Löwenstein M, Spallinger E (2009) First autochthonous case of canine Dirofilaria (Nochtiella) repens infection in Austria – a case report. Wien Tierärztl Mschr – Vet Med Austria 96:184 – 187.

  • 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(2 – 3):255 – 266.

    PubMed  Google Scholar 

  • Olmeda-García AS, Rodríguez-Rodríguez JA, Rojo-Vázquez FA (1993) Experimental transmission of Dipetalonema dracunculoides (Cobbold 1870) by Rhipicephalus sanguineus (Latreille 1806). Vet Parasitol 47(3 – 4):339 – 342.

    PubMed  Article  Google Scholar 

  • Olteanu G (1996) Dirofilarosis in man and animals in Romania. Parassitologia 38:360.

    Google Scholar 

  • Ortega-Mora LM, Gomez-Bautista M, Rojo-Vazquez F, Rodenas A, Guerrero J (1991) A survey of the prevalence of canine filariosis in Spain. Prev Vet Med 11:63 – 68.

    Article  Google Scholar 

  • Pantchev N, Norden N, Lorentzen L, Rossi M, Rossi U, Brand B, Dyachenko V (2009a) Current surveys on the prevalence and distribution of Dirofilaria spp. in dogs in Germany. Parasitol Res 105(Suppl 1):63 – 74.

    Article  Google Scholar 

  • Pantchev N, Schaper R, Limousin S, Norden N, Weise M, Lorentzen L (2009b) 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):101 – 114.

    Article  Google Scholar 

  • Papazahariadou MG, Koutinas AF, Rallis TS, Haralabidis ST (1994) Prevalence of microfilaraemia in episodic weakness and clinically normal dogs belonging to hunting breeds. J Helminthol 68:243 – 245.

    PubMed  Article  CAS  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(11):1323 – 1326.

    PubMed  CAS  Google Scholar 

  • Rishniw M, Barr SC, Simpson KW, Frongillo MF, Franz M, Dominguez Alpizar JL (2006) Discrimination between six species of canine microfilariae by a single polymerase chain reaction. Vet Parasitol 135(3 – 4):303 – 314.

    PubMed  Article  CAS  Google Scholar 

  • Rosenthal A, Coutelle O, Craxton M (1993) Large-scale production of DNA sequencing templates by microtitre format PCR. Nucleic Acids Res 21(1):173 – 174.

    PubMed  Article  CAS  Google Scholar 

  • Rzepczyk CM, Bishop CJ (1984) Immunological and ultrastructural aspects of the cell-mediated killing of Dirofilaria immitis microfilariae. Parasite Immunol 6(5):443 – 457.

    PubMed  Article  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(3):545 – 547.

    PubMed  Google Scholar 

  • Sassnau R, Dyachenko V, Pantchev N, Stöckel F, Dittmar K, Daugschies A (2009) Dirofilaria repens Befall in einem Schlittenhunde-Rudel im Land Brandenburg, Diagnose und Therapie der kaninen kutanen Dirofilariose. Tierärztl Prax 37:95 – 101.

    Google Scholar 

  • Solano-Gallego L, Llull J, Osso M, Hegarty B, Breitschwerdt E (2006) A serological study of exposure to arthropod-borne pathogens in dogs from northeastern Spain. Vet Res 37(2):231 – 244.

    PubMed  Article  Google Scholar 

  • Stenzenberger R, Gothe R (1999) Arthropodenübertragene parasitäre Infektionen und Zecken bei Hunden auf Teneriffa. Tierärztl Prax 27:47 – 52.

    Google Scholar 

  • Tarantini SM, Garippa G, Leoni A (1983) Attuale incidenza della filariasi del cane in Sardegna. Parassitologia 25:361 – 364.

    Google Scholar 

  • Tzanetou K, Gasteratos S, Pantazopoulou A, Gogou C, Konidaris D, Fragia K (2009) Subcutaneous dirofilariasis caused by Dirofilaria repens in Greece: a case report. J Cutan Pathol 36(8):892 – 895.

    PubMed  Article  Google Scholar 

  • Webber WAF, Hawking F (1955) Experimental maintenance of Dirofilaria repens and Dirofilaria immitis in dogs. Exp Parasitol 4:143 – 164.

    PubMed  Article  CAS  Google Scholar 

  • Weil GJ, Malane MS, Powers KG (1984) Detection of circulating parasite antigens in canine dirofilariasis by counterimmunoelectrophoresis. Am J Trop Med Hyg 33(3):425 – 430.

    PubMed  CAS  Google Scholar 

  • Weil GJ (1987) Dirofilaria immitis: identification and partial characterization of parasite antigens in the serum of infected dogs. Exp Parasitol 64(2):244 – 251.

    PubMed  Article  CAS  Google Scholar 

  • Weise M (2004) Reisetiermedizinisch und epidemiologisch wichtige Arten der kaninen Parasitenfauna in europäischen Anrainerstaaten des Mittelmeeres und in Portugal für Hunde in Deutschland – eine Literaturstudie. Inaugural-Dissertation, Ludwig-Maximilians-Universität München, p 293.

  • Zahler M, Glaser B, Gothe R (1997): Imported parasites in dogs: Dirofilaria repens and Dipetalonema reconditum. Tierärztl Prax 25(4):388 – 392.

    PubMed  CAS  Google Scholar 

  • Zivicnjak T, Martinkovic F, Beck FR (2007) Canine dirofilariosis in Croatia: let’s face it. Abstract Book of the First European Dirofilaria Days, 22 – 25 February, Zagreb, Croatia, p 35.

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Correspondence to Nikola Pantchev.

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Pantchev, N., Etzold, M., Daugschies, A. et al. Diagnosis of Imported Canine Filarial Infections in Germany 2008 – 2010. Parasitol Res 109, 61–76 (2011). https://doi.org/10.1007/s00436-011-2403-7

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  • DOI: https://doi.org/10.1007/s00436-011-2403-7

Keywords

  • Canis
  • Imidacloprid
  • Babesia
  • Moxidectin
  • Filarial Infection