Skip to main content
SpringerLink
Log in

Detection of Dirofilaria repens and Dirofilaria immitis DNA in mosquitoes from Belarus

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

An Erratum to this article was published on 02 June 2016

Abstract

During the last two decades, Belarus faces an increase of human cases of Dirofilaria (Nematoda, Spirurida, Onchocercidae) infections. However, comprehensive analyses explaining this development and the identification of mosquito vector species are missing. Here, we present results using temperature data from Belarus and show that the annual number of human Dirofilaria cases is significantly correlated with the yearly average temperatures (Spearman’s rho = 0.49, p < 0.05) and the average sum of potential Dirofilaria transmission days (Spearman’s rho = 0.46, p < 0.05), suggesting that autochthonous transmission is at least in part responsible for the increasing number of clinical Dirofilaria cases in the country. In addition, 467 female mosquitoes were collected from different sampling sites in the regions of Brest and Minsk, which were analyzed by molecular methods for the presence of Dirofilaria repens and Dirofilaria immitis DNA, respectively. Two pools (5.56 %) were tested positive for Dirofilaria (estimated infection rate per 100 specimens = 0.44, 95 % confidence interval = 0.08–1.43), comprising one Anopheles claviger s.l. pool that was positive for D. repens and one Culex pipiens s.l./Culex torrentium pool positive for D. immitis DNA. This, to our knowledge, is the first molecular evidence for the presence of Dirofilaria in mosquitoes from Belarus, suggesting a high probability of autochthonous Dirofilaria transmission in the country.

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
Fig. 2

Similar content being viewed by others

References

  • Becker N, Petrić D, Zgomba M, Boase C, Madon M, Dahl K, Kaiser A (2010) Mosquitoes and their control, 2nd edn. Springer, Heidelberg

    Book  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. Parasit Res 112:3465–3470

    Article  Google Scholar 

  • Bocková E, Iglódyová A, Kočišová A (2015) Potential mosquito (Diptera:Culicidae) vector of Dirofilaria repens and Dirofilaria immitis in urban areas of Eastern Slovakia. Parasit Res 114:4487–4492

    Article  Google Scholar 

  • Borkowski PK, Rymkiewicz G, Golebiewska J, Nestoros N, Romejko-Jarosinska J, Zarnowska-Prymek H, Masny A, Palucki J, Cielecka D (2014) The first case of human autochtonous subconjunctival dirofilariosis in Poland and MALT lymphoma as possible consequence of this parasitosis. Infect Agents Cancer 10:1. doi:10.1186/1750-9378-10-1

    Article  Google Scholar 

  • Bronshteyn AM, Malyshev NA, Jarov SN, Fedianina LV, Frolova АА, Supriaga VG, Luchshev VI (2013) A first autochthonous human case of the long standing microfilaraemia due to Dirofilaria repens in Russia and a first experience of combined therapy of dirofilariasis repens. Epidemiol Infect Dis 3:47–52 (in Russian)

    Google Scholar 

  • Cancrini G, Kramer L (2001) Insect vectors of Dirofilaria spp. In: Simón F, Genchi C (eds) Heartworm infection in humans and animals. Universidad de Salamanca, Salamanca, pp 63–82

    Google Scholar 

  • Carpova GN (2010) Physical geography of Belarus: a course of lectures, 2nd edn. Gomel State University, Gomel (in Russian)

    Google Scholar 

  • Chistenko GN, Vedenkov AL, Dronina AM, Semizhon OA (2013) Human dirofilariasis. Med Jurnal 3:30–33 (in Russian)

    Google Scholar 

  • Cielecka D, Żarnowska-Prymek H, Masny A, Salamatin R, Wesołowska M, Gołąb E (2012) Human dirofilariasis in Poland: the first cases of autochthonous infections with Dirofilaria repens. Ann Agric Environ Med 19(3):445–450

    PubMed  Google Scholar 

  • Fedianina LV (2010) Human dirofilariasis in Russia. Med Parazitol 2:43–44 (in Russian)

    Google Scholar 

  • Fedianina LV, Frolova AA, Pliushcheva GL, Chernyshenko AI, Morozov EN, Rakova VM (2011) Cases confirming the concept that the human being is a facultative host of Dirofilaria repens. Med Parazitol 4:37–38 (in Russian)

    Google Scholar 

  • Fedianina LV, Shatova SM, Rakova VM, Shaĭtanov VM, Lebedeva MN, Frolova AA, Morozov EN, Morozova LF (2013) Microfilaraemia in human dirofilariasis caused by Dirofilaria repens Raiet et Henry, 1911. A case report. Med Parazitol 2:3–7, in Russian

    Google Scholar 

  • Genchi C, Rinaldi L, Cascone C, Mortarino M, Cringoli G (2005) Is heartworm disease really spreading in Europe? Vet Parasitol 133:137–148

    Article  PubMed  Google Scholar 

  • Haylock MR, Hofstra N, Klein Tank AMG, Klok EJ, Jones PD, New M (2008) A European daily high-resolution gridded dataset of surface temperature and precipitation. J Geophys Res Atmos 113:D20119

    Article  Google Scholar 

  • Kartashev V, Tverdokhlebova T, Korzan A, Vedenkov A, Simón L, Gonzalez-Miguel J, Morchón R, Siles-Lucas M, Simón F (2015) Human subcutaneous/ocular dirofilariasis in the Russian Federation and Belarus, 1997–2013. Int J Infect Dis 33:209–211

    Article  PubMed  Google Scholar 

  • Mantovani A, Restani R (1965) Ricerche sui possibili artropodi vettori di Dirofilaria repens in alcune provincie dell Italia céntrale. Parassitologia 7:109–116

    Google Scholar 

  • Melbarde-Gorkusa I, Abolins A, Strumfa I, Martinsons A, Gardovskis J (2011) Human dirofilariasis in Latvia—the first case in surgical practice. Acta Chir Latv 11:172–174

    Google Scholar 

  • (MHRB) Ministry of Health of the Republic of Belarus 2014. Instruction on the prevention of dirofilariasis. Borisov Zonal Center of Hygiene and Epidemiology. http://www.gigbor.by/Norm_doc/TNPA/paraziti.doc. Accessed 29 Dec 2015 (in Russian)

  • Naralenkova E (2004) Notification of cases of dirofilariasis in the Gomel region. Med Parazitol 2:49–51 (in Russian)

    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  PubMed Central  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

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Pantchev N, Etzold M, Daugschies A, Dyachenko V (2011) Diagnosis of imported canine filarial infections in Germany 2008–2010. Parasit Res 109:61–76

    Article  Google Scholar 

  • Poppert S, Hodapp M, Krüger A, Hegasy G, Niesen WD, Kern WV, Tannich E (2009) Dirofilaria repens infection and concomitant meningoencephalitis. Emerg Infect Dis 15:1844–1846

    Article  PubMed  PubMed Central  Google Scholar 

  • R Core Team. R (2015) A language and environment for statistical computing [Internet]. R Foundation for Statistical Computing, Vienna, http://www.R-project.org/ Accessed 1 Dec 2015

    Google Scholar 

  • Rudolf I, Šebesta O, Mendel J, Betášová L, Bocková E, Jedličková P, Venclíková K, Blažejová H, Šikutová S, Hubálek Z (2014) Zoonotic Dirofilaria repens (Nematoda: Filarioidea) in Aedes vexans mosquitoes, Czech Republic. Parasit Res 113:4663–4667

    Article  Google Scholar 

  • Sałamatin RV, Pavlikovska TM, Sagach OS, Nikolayenko SM, Kornyushin VV, Kharchenko V, Masny A, Cielecka D, Konieczna-Sałamatin J, Conn DB, Golab E (2014) Human Dirofilaria repens infection in Ukraine (1997–2013). In: Fok E, Kucsera I (eds) Fourth European Dirofilaria and Angiostrongylus Days. Hungarian Society of Parasitologists, Budapest, p 80

    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. Parasit Res 112:2647–2652

    Article  CAS  Google Scholar 

  • Sassnau R, Czajka C, Kronefeld M, Werner D, Genchi C, Tannich E, Kampen H (2014) Dirofilaria repens and Dirofilaria immitis DNA findings in mosquitoes in Germany: temperature data allow autochthonous extrinsic development. Parasit Res 113:3057–3061

    Article  CAS  Google Scholar 

  • Schaffner F, Angel G, Geoffrey B, Hervy J-P, Rhaiem A, Brunhes J (2001) The mosquitoes of Europe. CD-ROM. Institut de Recherche pour le Développement/Entente interdépartementale pour la démoustication du littoral (EID) Méditerrannée, Montpellier

    Google Scholar 

  • Sergiev VP, Supriaga VG, Morozov EN, Zhukova LA (2009) Human dirofilariasis: diagnosis and the pattern of pathogen-host relations. Med Parazitol 3:3–6 (in Russian)

    Google Scholar 

  • Shimalov VV, Pen’kevich VA (2012) Helminth fauna of the wolf (Canis lupus Linnaeus, 1758) in Belorussian Polesie. Parazitologiia 46:118–126 (in Russian)

    CAS  PubMed  Google Scholar 

  • Simón F, Siles-Lucas M, Morchón R, González-Miguel J, Mellado I, Carretón E, Montoya-Alonso JA (2012) Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clin Microbiol Rev 25:507–544

    Article  PubMed  PubMed Central  Google Scholar 

  • Tappe D, Plauth M, Bauer T, Muntau B, Dießel L, Tannich E, Herrmann-Trost P (2014) A case of autochthonous human Dirofilaria infection, Germany, March 2014. Euro Surveill 19:2–4

    CAS  PubMed  Google Scholar 

  • Tasić A, Rossi L, Tasić S, Miladinović-Tasić N, Ilić T, Dimitrijević S (2008) Survey of canine dirofilariasis in Vojvodina, Serbia. Parasit Res 103:1297–1302

    Article  Google Scholar 

  • Tereshkina NV, Truhan MN, Kaplich VM (1998) Distribution of bloodsucking dipterous insects (Diptera: Culicidae, Simuliidae, Tabanidae) in ecosystems of Polesie State Radiation Ecological Reserve. In: Parfenov VI (ed). The 10th anniversary of the Polesie State Radiation Ecological Reserve. Minsk. pp. 179–182 (in Russian)

  • Volkova TV (2008) The mosquitoes (Diptera, Culicidae) of urban landscapes of Belarus. Dissertation, Institute of Zoology of NAS Belarus (in Russian)

  • Volkova TV, Tereshkina NV (2009) Peculiarities of the mosquito larval (Diptera, Culicidae) biotope distributions in urban areas of Belarus. Vestnik MSU 1:13–14 (in Russian)

    Google Scholar 

  • Volkova TV, Aksenova EA, Yashkova SE (2013) The current state of knowledge of the mosquitoes from the genus Anopheles (Diptera, Culicidae) in Belarusian Polesie. In: Medvedev SG (ed) Fundamental and applied aspects of study the parasitic arthropods in the XXI century. Zoological Institute RAS, St. Petersburg, pp 49–52 (in Russian)

    Google Scholar 

  • Zhang B, Bilder C, Biggerstaff B, Schaarschmidt F (2012) binGroup: evaluation and experimental design for binomial group testing. http://CRAN.R-project.org/package=binGroup. Accessed 1 Dec 2015

Download references

Acknowledgments

This work was partially supported by EurNegVec COST Action TD1303. We acknowledge the E-OBS dataset from the EU-FP6 project ENSEMBLES (http://ensembles-eu.metoffice.com) and the data providers in the ECA&D project (http://www.ecad.eu).

Author information

Authors and Affiliations

  1. Institute of Zoology, Academy of Sciences of Moldova, Chisinau, Moldova

    Tatiana Șuleșco

  2. Scientific and Practical Center of the National Academy of Sciences of Belarus for Biological Resources, Minsk, Belarus

    Tatiana Volkova

  3. Ministry of Health of the Republic of Belarus, State Republican Center of Hygiene, Epidemiology and Public Health, Minsk, Belarus

    Svetlana Yashkova

  4. Bernhard Nocht Institute for Tropical Medicine, WHO Collaborating Centre for Arbovirus and Haemorrhagic Fever Reference and Research National Reference Centre for Tropical Infectious Diseases, Bernhard-Nocht-Straße 74, 20359, Hamburg, Germany

    Alexandru Tomazatos, Heidrun von Thien, Renke Lühken & Egbert Tannich

  5. Centre for Infection Research (DZIF), partner site Hamburg-Luebeck-Borstel, Hamburg, Germany

    Egbert Tannich

Authors
  1. Tatiana Șuleșco
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tatiana Volkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Svetlana Yashkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexandru Tomazatos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Heidrun von Thien
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Renke Lühken
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Egbert Tannich
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Renke Lühken.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Șuleșco, T., Volkova, T., Yashkova, S. et al. Detection of Dirofilaria repens and Dirofilaria immitis DNA in mosquitoes from Belarus. Parasitol Res 115, 3535–3541 (2016). https://doi.org/10.1007/s00436-016-5118-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-016-5118-y

Keywords

Search

Navigation