Skip to main content

First Molecular Detection of Dirofilaria immitis and D. repens in Dogs from Kyrgyzstan

Abstract

Background

Dirofilaria immitis and Dirofilaria repens are the causative agents of cardiopulmonary and subcutaneous dirofilariosis, respectively. This neglected disease mainly seen in dogs, cats and wild carnivores is re-emerging recent years. No study was conducted on dirofilariosis in dogs in Kyrgyzstan.

Purpose

The goal of this study was to investigate Dirofilaria species using PCR and sequencing in dogs from Kyrgyzstan.

Method

Dirofilaria spp. infection in dogs was screened via convential PCR and sequencing in 337 dogs from Kyrgyzstan.

Result

The overall prevalence of Dirofilaria spp. was 0.59% (2/337): DNA of D. immitis was detected in one sample and DNA of D. repens in second positive sample. In second sample, parallel co-infection of D. repens with Wolbachia was also found. While D. immitis sequence showed 98.70–100% similarity with previously reported sequences of D. immitis from dog blood, D. repens shared 100% identity with other sequences of D. repens.

Conclusion

These results provided first evidence for Dirofilaria spp. in Kyrgyzstan and emphasized the veterinary and medical importance.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Altay K, Aydin MF, Aytmirzakizi A, Jumakanova Z, Cunusova A, Dumanli N (2019) Molecular survey of hepatozoonosis in natural infected dogs: first detection and molecular characterisation of Hepatozoon canis in Kyrgyzstan. Kafkas Univ Vet Fak Derg 25(1):77–81. https://doi.org/10.9775/kvfd.2018.20352

    Article  Google Scholar 

  2. Altay K, Aydin MF, Aytmirzakizi A, Jumakanova Z, Cunusova A, Dumanli N (2020) First molecular evidence for Mycoplasma haemocanis and Candidatus Mycoplasma haematoparvum in asymptomatic shelter dogs in Kyrgyzstan. Kafkas Univ Vet Fak Derg 26(1):143–146. https://doi.org/10.9775/kvfd.2019.22196

    Article  Google Scholar 

  3. Ataş AD, Altay K, Alim A, Özkan E (2018) Survey of Dirofilaria immitis in dogs from Sivas Province in the Central Anatolia Region of Turkey. Turk J Vet Anim Sci 42(2):130–134. https://doi.org/10.3906/vet-1707-93

    CAS  Article  Google Scholar 

  4. Bamorovat M, Sharifi I, Harandi MF, Nasibi S, Sadeghi B, Khedri J, Mohammadi MA (2017) Parasitological, serological and molecular study of Dirofilaria immitis in domestic dogs, southeastern Iran. Iran J Parasitol 12(2):260–266

    PubMed  PubMed Central  Google Scholar 

  5. Bekker CP, de Vos S, Taoufik A, Sparagano OA, Jongejan F (2002) Simultaneus detection of Anaplasma and Ehrlichia species in ruminants and detection of Ehrlichia ruminantum in Amblyomma variegatum ticks by reverse line blot hybridization. Vet Mic 89(2–3):223–228. https://doi.org/10.1016/s0378-1135(02)00179-7

    CAS  Article  Google Scholar 

  6. Capelli G, Genchi C, Baneth G, Bourdeau P, Brianti E, Cardoso L, Maia C (2018) Recent advances on Dirofilaria repens in dogs and humans in Europe. Parasite Vector 11(1):663. https://doi.org/10.1186/s13071-018-3205-x

    Article  Google Scholar 

  7. Casiraghi M, Anderson TJC, Bandi C, Bazzocchi C, Genchi C (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122:93–103. https://doi.org/10.1017/s0031182000007149

    CAS  Article  Google Scholar 

  8. Dearsley EJ, O’Handley RM, Caraguel CGB (2019) Is canine heartworm (Dirofilaria immitis) endemic to South Australia? Aust Vet J 97(6):191–196. https://doi.org/10.1111/avj.12814

    CAS  Article  Google Scholar 

  9. Diakou A, Kapantaidakis E, Tamvakis A, Giannakis V, Strus N (2016) Dirofilaria infections in dogs in different areas of Greece. Parasite Vector 9(1):508. https://doi.org/10.1186/s13071-016-1797-6

    Article  Google Scholar 

  10. Ferreira C, Afonso A, Calado M, Maurício I, Alho AM, Meireles J, Belo S (2017) Molecular characterization of Dirofilaria spp. circulating in Portugal. Parasite Vector 10(1):250. https://doi.org/10.1186/s13071-017-2180-y

    CAS  Article  Google Scholar 

  11. Genchi C, Kramer L (2017) Subcutaneous dirofilariosis (Dirofilaria repens): an infection spreading throughout the old world. Parasite Vector 10(2):517. https://doi.org/10.1186/s13071-017-2434-8

    Article  Google Scholar 

  12. Genchi M, Rinaldi L, Venco L, Cringoli G, Vismarra A, Kramer L (2019) Dirofilaria immitis and D. repens in dog and cat: a questionnaire study in Italy. Vet Parasitol 267:26–31. https://doi.org/10.1016/j.vetpar.2019.01.014

    Article  Google Scholar 

  13. Guven E, Avcioglu H, Cengiz S, Hayirli A (2017) Vector-borne pathogens in stray dogs in Northeastern Turkey. Vector Borne Zoonotic Dis 17(8):610–617. https://doi.org/10.1089/vbz.2017.2128

    Article  PubMed  PubMed Central  Google Scholar 

  14. Hou H, Cao L, Ren W, Wang D, Ding H, You J, Zhang X (2017) Seroprevalence of Dirofilaria immitis in cats from Liaoning Province. Northeast China Korean J Parasitol 55(6):673–677. https://doi.org/10.3347/kjp.2017.55.6.673

    Article  Google Scholar 

  15. Ionică AM, Matei IA, D’Amico G, Bel LV, Dumitrache MO, Modrý D, Mihalca AD (2017) Dirofilaria immitis and D. repens show circadian co-periodicity in naturally co-infected dogs. Parasite Vector 10(1):116. https://doi.org/10.1186/s13071-017-2055-2

    Article  Google Scholar 

  16. Kozek WJ (2005) What is new in the Wolbachia/Dirofilaria interaction? Vet Parasitol 133(2–3):127–132. https://doi.org/10.1016/j.vetpar.2005.02.005

    Article  Google Scholar 

  17. Kravchenko V, Itin G, Kartashev V, Ermakov A, Kartashov S, Diosdado A, Simón F (2016) Dirofilaria immitis and D. repens in sylvatic reservoirs of Krasnodar Krai (Russian Federation). Vet Parasitol Reg Stud Rep 6:35–38. https://doi.org/10.1016/j.vprsr.2016.08.004

    Article  Google Scholar 

  18. Maia C, Lorentz S, Cardoso L, Otranto D, Naucke TJ (2016) Detection of Dirofilaria repens microfilariae in a dog from Portugal. Parasitol Res 115(1):441–443. https://doi.org/10.1007/s00436-015-4796-1

    Article  Google Scholar 

  19. Malik D, Amaraneni A, Singh S, Roach R (2016) Man's best friend: how humans can develop Dirofilaria immitis infections. IDCases 4:43–45. https://doi.org/10.1016/j.idcr.2016.03.003

    Article  PubMed  PubMed Central  Google Scholar 

  20. Marcos R, Pereira C, Maia JP, Santos M, Luzzago C, Lauzi S, Puente-Payo P (2017) The occurrence of the filarial nematode Dirofilaria repens in canine hosts from Maio Island. Cape Verde J Helminthol 91(1):87–90. https://doi.org/10.1017/S0022149X16000067

    CAS  Article  Google Scholar 

  21. Monobe MM, da Silva RC, Junior JPA, Takahira RK (2017) Microfilaruria by Dirofilaria immitis in a dog: a rare clinical pathological finding. J Parasit Dis 41(3):805–808. https://doi.org/10.1007/s12639-017-0892-8

    Article  PubMed  PubMed Central  Google Scholar 

  22. Oh IY, Kim KT, Sung HJ (2017) Molecular detection of Dirofilaria immitis specific gene from infected dog blood sample using polymerase chain reaction. Iran J Parasitol 12(3):433–440

    PubMed  PubMed Central  Google Scholar 

  23. Paździor-Czapula K, Otrocka-Domagała I, Myrdek P, Mikiewicz M, Gesek M (2018) Dirofilaria repens—an etiological factor or an incidental finding in cytologic and histopathologic biopsies from dogs. Vet Clin Pathol 47(2):307–311. https://doi.org/10.1111/vcp.12597

    Article  Google Scholar 

  24. Pedram N, Tabrizi AS, Hosseinzadeh S, Pourmontaseri M, Rakhshandehroo E (2019) Prevalence of Dirofilaria immitis and Dirofilaria repens in outdoor dogs in Tehran Province. Iran Comp Clin Path 28(4):1165–1169. https://doi.org/10.1007/s00580-019-02964-5

    Article  Google Scholar 

  25. Pfarr KM, Hoerauf AM (2006) Antibiotics which target the Wolbachia endosymbionts of filarial parasites: a new strategy for control of filariasis and amelioration of pathology. Mini Rev Med Chem 6:203–210. https://doi.org/10.2174/138955706775475984

    CAS  Article  Google Scholar 

  26. Ramos-Lopez S, León-Galván MF, Salas-Alatorre M, Lechuga-Arana AA, Valencia-Posadas M, Gutiérrez-Chávez AJ (2016) First molecular identification of Dirofilaria repens in a dog blood sample from Guanajuato. Mexico Vector Borne Zoonotic Dis 16(11):734–736. https://doi.org/10.1089/vbz.2016.1948

    Article  Google Scholar 

  27. Raoof P, Garedaghi Y (2017) Investigation of infection with Dirofilaria immitis parasite in stray dogs in Tabriz city of Iran. Livest Sci 8:38–42

    Google Scholar 

  28. 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 135:303–314. https://doi.org/10.1016/j.vetpar.2005.10.013

    CAS  Article  Google Scholar 

  29. Rjeibi MR, Rouatbi M, Mabrouk M, Tabib I, Rekik M, Gharbi M (2017) Molecular study of Dirofilaria immitis and Dirofilaria repens in dogs from Tunisia. Transbound Emerg Dis 64(5):1505–1509. https://doi.org/10.1111/tbed.12541

    CAS  Article  Google Scholar 

  30. Sabūnas V, Radzijevskaja J, Sakalauskas P, Paulauskas A (2019) First report of heartworm (Dirofilaria immitis) infection in an imported dog in Lithuania. Helminthologia 56(1):57–61. https://doi.org/10.2478/helm-2018-0036

    Article  PubMed  PubMed Central  Google Scholar 

  31. Sabūnas V, Radzijevskaja J, Sakalauskas P, Petkevičius S, Karvelienė B, Žiliukienė J, Paulauskas A (2019) Dirofilaria repens in dogs and humans in Lithuania. Parasite Vector 12(1):177. https://doi.org/10.1186/s13071-019-3406-y

    Article  Google Scholar 

  32. Sari B, Tasci GT, Kilic Y (2013) Seroprevalence of Dirofilaria immitis, Ehrlichia canis and Borrelia burgdorferi in dogs in Iğdır Province. Turkey Kafkas Univ Vet Fak Derg 19(5):735–739. https://doi.org/10.9775/kvfd.2012.8466

    Article  Google Scholar 

  33. Sassnau R, Daugschies A, Lendner M, Genchi C (2014) Climate suitability for the transmission of Dirofilaria immitis and D. repens in Germany. Vet Parasitol 205(1–2):239–245. https://doi.org/10.1016/j.vetpar.2014.06.034

    CAS  Article  Google Scholar 

  34. Satjawongvanit H, Phumee A, Tiawsirisup S, Sungpradit S, Brownell N, Siriyasatien P, Preativatanyou K (2019) Molecular analysis of Canine Filaria and its Wolbachia Endosymbionts in domestic dogs collected from Two Animal University Hospitals in Bangkok Metropolitan Region. Thail Pathog 8:114. https://doi.org/10.3390/pathogens8030114

    CAS  Article  Google Scholar 

  35. Schouls LM, Van de Pol I, Rijpkema SG, Schot CS (1999) Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks. J Clin Microbiol 37(7):2215–2222

    CAS  Article  Google Scholar 

  36. Shaikevich E, Bogacheva A, Ganushkina L (2019) Dirofilaria and Wolbachia in mosquitoes (Diptera: Culicidae) in central European Russia and on the Black Sea coast. Parasite 26:2. https://doi.org/10.1051/parasite/2019002

    Article  PubMed  PubMed Central  Google Scholar 

  37. Simsek S, Ciftci AT (2016) Serological and molecular detection of Dirofilaria species in stray dogs and investigation of Wolbachia DNA by PCR in Turkey. J Arthropod Borne Dis 10(4):445–453

    PubMed  PubMed Central  Google Scholar 

  38. Tahir D, Bittar F, Barré-Cardi H, Sow D, Dahmani M, Mediannikov O, Parola P (2017) Molecular survey of Dirofilaria immitis and Dirofilaria repens by new real-time TaqMan® PCR assay in dogs and mosquitoes (Diptera: Culicidae) in Corsica (France). Vet Parasitol 235:1–7. https://doi.org/10.1016/j.vetpar.2017.01.002

    CAS  Article  Google Scholar 

  39. Tahir D, Damene H, Davoust B, Parola P (2017) First molecular detection of Dirofilaria immitis (Spirurida: Onchocercidae) infection in dogs from Northern Algeria. Comp Immunol Microbiol Infect Dis 51:66–68. https://doi.org/10.1016/j.cimid.2017.04.001

    Article  Google Scholar 

  40. Torres-Chable OM, Baak-Baak CM, Cigarroa-Toledo N, Blitvich BJ, Brito-Argaez LG, Alvarado-Kantun YN, Machain-Williams CI (2018) Molecular detection of Dirofilaria immitis in dogs and mosquitoes in Tabasco, Mexico. J Vector Borne Dis 55(2):151–158. https://doi.org/10.4103/0972-9062.242563

    Article  Google Scholar 

  41. Ural K, Gultekin M, Atasoy A, Ulutas B (2014) Spatial distribution of vector borne disease agents in dogs in Aegean region. Turkey Rev MVZ Cordoba 19(2):4086–4098

    CAS  Article  Google Scholar 

  42. Vezzani D, Mesplet M, Eiras DF, María F, Fontanarrosa MF, Schnittger L (2011) PCR detection of Dirofilaria immitis in Aedes aegypti and Culex pipiens from urban temperate Argentina. Parasitol Res 108:985–989. https://doi.org/10.1007/s00436-010-2142-1

    Article  Google Scholar 

  43. Wang S, Zhang N, Zhang Z, Wang D, Yao Z, Zhang H, Liu S (2016) Prevalence of Dirofilaria immitis infection in dogs in Henan province, central China. Parasite 23:43. https://doi.org/10.1051/parasite/2016054

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Viktória Čabanová (Slovak Academy of Sciences, Institute of Parasitology, Košice 040 01, Slovakia) for providing positive control DNA of D. repens. Also, we are grateful to animal shelter staffs and Kyrgyz-Turkish Manas University Veterinary Teaching Hospital staffs for their kind help during sample collection.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mehmet Fatih Aydın.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethic statement

Ethics committee approval was received from the Animal Experimentation Ethics Committee of Kyrgyz-Turkish Manas University (Document No: 29.06.2017/2017-06/01).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Aydın, M.F., Altay, K., Aytmirzakizi, A. et al. First Molecular Detection of Dirofilaria immitis and D. repens in Dogs from Kyrgyzstan. Acta Parasit. 65, 949–953 (2020). https://doi.org/10.1007/s11686-020-00245-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11686-020-00245-8

Keywords

  • Dirofilaria immitis
  • Dirofilaria repens
  • Kyrgyzstan
  • Dog
  • Vector-borne diseases
  • PCR
  • Sequencing