Parasitology Research

, Volume 113, Issue 9, pp 3281–3285 | Cite as

First findings and prevalence of adult heartworms (Dirofilaria immitis) in wild carnivores from Serbia

  • Aleksandra Penezić
  • Sanja Selaković
  • Ivan Pavlović
  • Duško Ćirović
Original Paper


Heartworm (Dirofilaria immitis) is a parasitic roundworm that causes a zoonotic disease known as dirofilariosis. Little is known about the role of wild carnivores serving as reservoirs in nature. Therefore, we examined 738 hearts and lungs of free ranging wild carnivores from Serbia to determine the presence of adult heartworms. During the period 2009–2013, the prevalence in golden jackals (Canis aureus) was 7.32 %, in red foxes (Vulpes vulpes) 1.55 %, in wolves (Canis lupus) 1.43 %, and in wild cats (Felis silvestris) 7.69 %. No adult heartworm specimens were found in beech martens (Martes foina), stone martens (Martes martes), European polecats (Mustela putorius), badgers (Meles meles) or otter (Lutra lutra). The highest recorded prevalence was in 2013 (7.30 %) and the lowest in 2012 (1.6 %). In jackals, the prevalence was higher in males (10 %) than in females (4.06 %), while in foxes the prevalence was 1.75 % in males and 1.26 % in females. The most infected host was a wolf in which 37 adult specimens were found. Because of the potentially significant role in the life cycle of D. immitis, populations of wild carnivores in Europe should be further examined and tested for heartworm infections.


Dirofilaria immitis Heartworm Serbia Free-ranging carnivores 



This study was supported by a grant from the Ministry of Education Science and Technological Development of the Republic of Serbia (Project No. OI 173006). Authors wish to express their gratitude to all collaborators in the field who helped in collecting the material for this study.


  1. Anderson RC (2000) Nematode parasites of vertebrates, their development and transmission. CABI Publishing 2nd Edition, pp 650Google Scholar
  2. Arnold J, Humer A, Heltai M, Murariu D, Spassov N, Hackländer K (2012) Current status and distribution of golden jackals Canis aureus in Europe. Mammal Rev 42:1–11CrossRefGoogle Scholar
  3. Bargues MD, Morchón R, Latorre JM, Cancrini G, Mas-Coma S, Simón F (2006) Ribosomal DNA second internal transcribed spacer sequence studies of Culicid vectors from an endemic area of Dirofilaria immitis in Spain. Parasitol Res 99(3):205–213PubMedCrossRefGoogle Scholar
  4. Barriga OO (1982) Dirofilariosis. In: Steele JH, Schultz MG (eds) Handbook series in zoonoses, vol 2. CRC Press Inc, Boca Raton, pp 93–110Google Scholar
  5. Contesse P, Hegglin D, Gloor S, Bontadina F, Deplazes P (2004) The diet of urban foxes (Vulpes vulpes) and the availability of anthropogenic food in the city of Zurich Switzerland. Mamm Biol 69:81–95Google Scholar
  6. Ćirović D, Penezić A, Milenković M, Paunović M (2013) Winter diet composition of the golden jackal (Canis aureus L., 1758) in Serbia. Mamm. Biol. 10.1016/j.mambio.2013.11.003
  7. Džamić AM, Čolović IV, Arsić-Arsenijević VS, Stepanović S, Boričić I, Džamić Z, Mitrović SM, Rašić DM, Stefanović I, Latković Z, Kranjčić-Zec IF (2009) Human Dirofilaria repens infection in Serbia. J Helminth 83:129–137PubMedCrossRefGoogle Scholar
  8. Eira C, Vingada J, Torres J, Miquel J (2006) The helminth community of the red fox, Vulpes vulpes, in Dunas de Mira (Portugal) and its effect on host condition. Wildlife Biol Practice 2:26–36CrossRefGoogle Scholar
  9. Georgieva D, Kirkova Z, Ivanov A (2001) A study on the incidence and diagnostics of dirofilariosis (Heartworm disease) in carnivores. Bulg J Vet Med 4:231–237Google Scholar
  10. Gómez-Merino E, Chiner E, Signes-Costa J, Arriero JM, Zaragozí MV, Onrubia JA, Mayol MJ (2002) Pulmonary dirofilariosis mimicking lung cancer. Monaldi Arch Chest Dis 57:33–34PubMedGoogle Scholar
  11. Gortázar C, Castillo Hernández JA, Lucientes Curdi J, Blanco JC, Arriolabengoa A, Calvete C (1994) Factors affecting Dirofilaria immitis prevalence in red foxes in northeastern Spain. J Wildlife Dis 30:545–547CrossRefGoogle Scholar
  12. Kirkova Z, Raychev E, Georgieva D (2011) Studies on feeding habits and parasitological status of red fox, golden jackal, wild cat and stone marten in Sredna gora, Bulgaria. Journal of Life Sciences 5:264–270Google Scholar
  13. Kusak J, Skrbinšek AM, Dj H (2005) Home ranges, movements, and activity of wolves (Canis lupus) in the Dalmatian part of Dinarids, Croatia. Eur J Wildl Res 51:254–262CrossRefGoogle Scholar
  14. Magi M, Calderini P, Gabrielli S, Dell’Omodarme M, Macchioni F, Prati MC, Cancrini G (2008) Vulpes vulpes: a possible wild reservoir for zoonotic filariae. Vector-borne zoonot 8:249–252CrossRefGoogle Scholar
  15. Milenković M (1997) Taxonomic–biogeographic status and ecological/economic significance of the wolf (Canis lupus Linnaeus 1758) in Yugoslavia. Dissertation, University of Belgrade, SerbiaGoogle Scholar
  16. Mulanovich EA, Mulanovich VE, Rolston KH (2008) A case of Dirofilaria pulmonary infection coexisting with lung cancer. J Infect 56:241–243PubMedCrossRefGoogle Scholar
  17. Muro A, Genchi C, Cordero M, Simón F (1999) Human dirofilariosis in the European Union. Parasitol Today 15:386–389PubMedCrossRefGoogle Scholar
  18. Okarma H, Jędrzejewski W, Schmidt K, Śnieżko S, Bunevich AN, Jędrzejewska B (1998) Home ranges of wolves in Białowieża Primeval Forest, Poland, compared with other Eurasian populations. J Mammal 79:842–852CrossRefGoogle Scholar
  19. Oriel TC, Eberhard ML (1998) Zoonotic filariaisis. Clin Microbiol Rev 11:366–381Google Scholar
  20. Pascucci I, Fico R, D’Angelo AR, Serini S, Cammà C (2007) First notification in Italy of cardiopulmonary filariosis (heartworm disease) in a wolf (Canis lupus). Vet Ital 43:843–850PubMedGoogle Scholar
  21. Šálek M, Červinka J, Banea OC, Krofel M, Ćirović D, Selanec I, Penezić A, Grill S, Riegert J (2013) Population densities and habitat use of the golden jackal (Canis aureus) in farmlands across the Balkan Peninsula. Eur J Wildlife Res. doi:10.1007/s10344-013-0765-0 Google Scholar
  22. Segovia JM, Torres J, Miquel J, Llaneza L, Feliu C (2001) Helminths in the wolf, Canis lupus, from north-western Spain. J Helminthol 75:183–192PubMedGoogle Scholar
  23. Simón F, Siles-Lucas M, Morchón R, González-Miguel J, Mellado I, Carretón E, Montoya-Alonso JA (2012) Human and animal dirofilariosis: the emergence of a zoonotic mosaic. Clin Microbiol Rev 25:507–544PubMedCentralPubMedCrossRefGoogle Scholar
  24. Tasić A, Rossi L, Tasić S, Miladinović-Tasić N, Ilić T, Dimitrijević S (2008) Survey of canine dirofilariasis in Vojvodina. Serbia Parasitol Res 103:1297–1302CrossRefGoogle Scholar
  25. Tasić A, Tasić-Otašević S, Gabrielli S, Miladinović-Tasić N, Ignjatović A, Djordjević J, Dimitrijević S, Cancrini G (2012) Canine Dirofilaria Infections in two uninvestigated areas of Serbia: epidemiological and genetic aspects. Vector-borne zoonot 12:1031–1035CrossRefGoogle Scholar
  26. Vezzani D, Mesplet M, Eiras DF, Fontanarrosa MF, Schnittger L (2011) PCR detection of Dirofilaria immitis in Aedes aegypti and Culex pipiens from urban temperate Argentina. Parasitol Res 108(4):985–989PubMedCrossRefGoogle Scholar
  27. Vujić A, Stefanović A, Dragičević I, Matijević T, Pejčić L, Knežević M, Krašić D, Veselić S (2010) Species composition and seasonal dynamics of mosquitoes (Diptera: Cuculidae) in flooded areas of Vojvodina, Serbia. Arch. Biol. Sci. Belgrade 62:1193–1206Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Aleksandra Penezić
    • 1
  • Sanja Selaković
    • 2
  • Ivan Pavlović
    • 3
  • Duško Ćirović
    • 1
  1. 1.Faculty of BiologyUniversity of BelgradeBelgradeSerbia
  2. 2.Faculty of Veterinary MedicineUniversity of UtrechtUtrechtNetherlands
  3. 3.Scientific Institute of Veterinary Medicine of SerbiaBelgradeSerbia

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