Skip to main content

Advertisement

SpringerLink
Log in

Filariasis in dogs brought to the Veterinary Teaching Hospital, University of Peradeniya, Sri Lanka

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

Abstract

Dirofilariasis is the predominant emerging zoonotic filariasis in the world. The two most frequent filarial worms that infect dogs are Dirofilaria repens and Dirofilaria immitis. This study reports filariasis among dogs brought to the Veterinary Teaching Hospital (VTH) at the University of Peradeniya and signifies the first molecular characterization of D. repens, responsible for an emerging zoonotic filarial disease in Sri Lanka. Blood samples were collected and were morphologically analyzed using Modified Knott’s Technique, followed by molecular analyses. The difference in filariasis prevalence among gender, breed, and age categories was analyzed using a chi-square test. Infection intensities were analyzed using the Mann–Whitney U test and the Kruskal Wallis test. The dogs were brought to the clinic for either vaccination and/or for a regular checkup, and most were sick having non-specific clinical signs. Among the 87 dogs tested, 27.6% were positive for Dirofilaria. Conventional PCR and bi-directional sequencing of genomic DNA of microscopically tested positive samples revealed that the species in Sri Lanka was D. repens. The infection was significantly higher in males (39.1%) than in females (14.6%; χ2 = 0.447, p = 0.011), though it is not significant between puppies (age < 1 year) and adult dogs. More crossbred dogs were infected compared to older and purebred dogs. There was no difference in intensity of infection based on their gender, age, or breed. Sequences obtained from the current study were unique and were only 63% identical to those of D. repens reported from South India. The high number of Dirofilaria infections in domestic dogs indicates a potential reservoir for emerging human dirofilariasis cases in Sri Lanka. Thus, morphological and molecular diagnosis, along with epidemiological assessment of these zoonoses, is critical for the formulation of effective public health programs and control mechanisms.

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
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

Data available on request due to privacy/ethical restrictions.

References

  • Abdul Cader MHM, Tharumarajah K, Rajendran K (1966) Filarial infection in domestic cats in Ceylon. Bull Indian Soc Malar & Other Commun Dis 3:155–158

    Google Scholar 

  • Abeysinghe AHMGB, Jiffry RAM, Perera WMM (2018) Human subcutaneous dirofilariasis: an increasing phenomenon in Sri Lanka. Sri Lanka J Surg 36:35. https://doi.org/10.4038/sljs.v36i1.8480

    Article  Google Scholar 

  • Alsarraf M, Levytska V, Mierzejewska EJ, Poliukhovych V, Rodo A, Alsarraf M, Kavalevich D, Dwużnik-Szarek D, Behnke JM, Bajer A (2021) Emerging risk of Dirofilaria spp . infection in Northeastern Europe : high prevalence of Dirofilaria repens in sledge dog kennels from the Baltic countries. Sci Rep 1–8. https://doi.org/10.1038/s41598-020-80208-1

  • Annual Health Bulletin (2015) Sri Lanka. (2017). Medical Statistics Unit, Ministry of Health, Nutrition and Indigenous Medicine. Nutrition and Indigenous Medicine 30:1–208

  • Bamorovat M, Sharifi I,  Harandi FM, 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 12:260–266

    Google Scholar 

  • Boonyapakorn C, Srikitjakarn L, Morakote N, Hoerchner F (2008) The epidemiology of Dirofilaria immitis infection in outpatient dogs at Chiang Mai University small animal hospital, Thailand. Southeast Asian J Trop Med Public Heal 39:33–38

    Google Scholar 

  • Borthakur SK, Deka DK, Islam S et al (2015) Prevalence and molecular epidemiological data on Dirofilaria immitis in dogs from Northeastern States of India. Sci World J 2015:1–7. https://doi.org/10.1155/2015/265385

  • Brunet K, Catroux M, Yera H et al (2020) Photo Quiz : Migrating Worm Naturally Exited through the Palate. J Clin Microbiol 58:1

  • Byeon KH, Kim BJ, Kim SM et al (2007) A serological survey of Dirofilaria immitis infection in pet dogs of Busan, Korea, and effects of chemoprophylaxis. Korean J Parasitol 45:27–32. https://doi.org/10.3347/kjp.2007.45.1.27

    Article  Google Scholar 

  • Chandrasekharan NV, Karunanayake HE, Franzen L et al (1994) Dirofilaria repens: cloning and characterization of a repeated DNA sequence for the diagnosis of Dirofilariasis in dogs, Canis familiaris. Exp Parasitol 78:279–286

    Article  CAS  Google Scholar 

  • Chandrasena TGAN, Premaratna R, Mallawaarachchi CH et al (2019) The diversity of human Dirofilariasis in Western Sri Lanka. Biomed Res Int 2019:1–7. https://doi.org/10.1155/2019/9209240

  • Cimpan AA, Baneth G, Nachum-Biala Y et al (2022) Dirofilaria repens predominates in shelter dogs from South Romania. Comp Immunol Microbiol Infect Dis 84:101793. https://doi.org/10.1016/j.cimid.2022.101793

    Article  CAS  Google Scholar 

  • Ciocan R, Dărăbuş G, Igna V (2010) Morphometric study of microfilariae of Dirofilaria spp. on dogs. Bull Univ Agric Sci Vet Med Cluj-Napoca - Vet Med 67:45–49. https://doi.org/10.15835/buasvmcn-vm:67:2:5920

  • Courtney CH, Zeng QY (2001) Relationship between microfilaria count and sensitivity of the direct smear for diagnosis of canine dirofilariosis. Vet Parasitol 94:199–204. https://doi.org/10.1016/S0304-4017(00)00377-0

    Article  CAS  Google Scholar 

  • Dasanayake R, Balendran T, Atapattu D, Iddawela D (2022) A study on canine dirofilariasis in selected areas of Sri Lanka. BMC Res Notes 15:1–6. https://doi.org/10.1186/s13104-022-06024-0

    Article  CAS  Google Scholar 

  • De Silva GPUP, Udugampola DS, Ekanayake EMIB et al (2021) An underrated differential diagnosis for subcutaneous lumps : 26 cases of subcutaneous Dirofilariasis. Sri Lanka J Surg 39:31–33. https://doi.org/10.4038/sljs.v39i2.8827

  • Dissanaike AS (1961) On some helminths of dogs in Colombo and their bearing on human infections, with a description of a new trematode Heterophyopsis yehi sp.nov. (Heterophyidae). Ceylon J Med Sci 10:1–12

    Google Scholar 

  • Dissanaike AS (1971) Human infections with Dirofilaria, a filarial parasite of animals in Ceylon, with a brief review of recent cases. Ceylon Med J 17:91–99

    Google Scholar 

  • Dissanaike AS (1979) Zoonotic aspects of filarial infections in man. Bull World Health Organ 57:349–357

    CAS  Google Scholar 

  • Dissanaike AS, Abeyewickreme W, Wijesundera MD et al (1997) Human dirofilariasis caused by Dirofilaria (Nochtiella) repens in Sri Lanka. Parassitologia 39:375–382

    CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an apptoach using the Bootstrap. Evolution (N Y) 39:783–791

    Google Scholar 

  • Gadahi JA, Arijo AG, Abubakar M et al (2008) Prevalence of blood parasites in stray and pet dogs in hyderabad area: comparative sensitivity of different diagnostic techniqes for the detection of microfilaria. Vet World 1:229–232

    Google Scholar 

  • Genchi C, Venco L, Genchi M (2007) Guideline for the laboratory diagnosis of canine and feline Dirofilaria infections. Mappe Parassitologiche 8:137–144

  • Gunathilaka N, Siriwardana S, Wijesooriya L, et al (2017) Subcutaneous dirofilariasis caused by Dirofilaria (Nochtiella) repens in Sri Lanka: a potential risk of transmitting human dirofilariasis . SAGE Open Med Case Rep 5:1–4. https://doi.org/10.1177/2050313x17701373

  • Hoch H, Strickland K (2008) Canine and Feline Dirofilariasis: life cycle, pathophysiology, and diagnosis. Compendium 30:133

    Google Scholar 

  • Iddawela D, Ehambaram K, Wickramasinghe S (2015) Human ocular dirofilariasis due to Dirofilaria repens in Sri Lanka. Asian Pac J Trop Med 8:1022–1026. https://doi.org/10.1016/j.apjtm.2015.11.010

    Article  Google Scholar 

  • Jayasinghe RD, Gunawardane SR, Sitheeque MAM, Wickramasinghe S (2015) A case report on oral subcutaneous Dirofilariasis. Case Rep Infect Dis 2015:1–4. https://doi.org/10.1155/2015/648278

    Article  Google Scholar 

  • Khedri J, Radfar MH, Borji H et al (2014) Canine heartworm in southeastern of Iran with review of disease distribution. Iran J Parasitol 9:560–567

    Google Scholar 

  • Krämer F, Schaper R, Schunack B et al (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. https://doi.org/10.1007/s00436-014-3985-7

    Article  Google Scholar 

  • Liotta JL, Sandhu GK, Rishniw M, Bowman DD (2013) Differentiation of the microfilariae of Dirofilaria immitis and Dirofilaria repens in stained blood films. J Parasitol 99:421–425. https://doi.org/10.1645/12-10.1

    Article  Google Scholar 

  • Mallawarachchi CH, Chandrasena NTGA, Wickramasinghe S et al (2018) A preliminary survey of filarial parasites in dogs and cats in Sri Lanka. PLoS ONE 13:1–11. https://doi.org/10.1371/journal.pone.0206633

    Article  CAS  Google Scholar 

  • Mallawarachchi CH, Chandrasena TGAN, Withanage GP et al (2021) Molecular characterization of a reemergent Brugia malayi parasite in Sri Lanka, Suggestive of a Novel Strain. Biomed Res Int 2021:1–7

    Article  Google Scholar 

  • Morchón R, Carretón E, González-Miguel J, Mellado-Hernández I (2012) Heartworm disease (Dirofilaria immitis) and their vectors in Europe - new distribution trends. Front Physiol 3:1–11. https://doi.org/10.3389/fphys.2012.00196

  • Pampiglione S, Canestri TG, Rivasi F (1995) Human dirofilariasis due to Dirofilaria (Nochtiella) repens: a review of world literature. Parassitologia 37:149–193

    CAS  Google Scholar 

  • Perera SJE (1956) Preliminary survey of the incidence of filariasis in dogs in Kandy District. Ceylon Vet J 4:22–24

    Google Scholar 

  • Rajapakshe RPAS, Perera WSR, Ihalamulla RL et al (2005) Study of dirofilariasis in a selected area in the Western Province. Ceylon Med J 50:58–61. https://doi.org/10.4038/cmj.v50i2.1570

    Article  CAS  Google Scholar 

  • Ratnatunga N, de Wijesundera M, S, (1999) Histopathological diagnosis of subcutaneous Driofilaria repens infection in humans. Southeast Asian J Trop Med Public Heal 30:375–378

    CAS  Google Scholar 

  • Ravindran R, Varghese S, Nair SN, et al (2014) Canine filarial infections in a human Brugia malayi endemic area of India. Biomed Res Int 2014:1–9. https://doi.org/10.1155/2014/630160

  • Rishniw M, Barr SC, Simpson KW et al (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

    Article  CAS  Google Scholar 

  • Sabu L, Devada K, Subramanian H (2005) Dirofilariosis in dogs & humans in Kerala. Indian J Med Res 121:691–693

    Google Scholar 

  • Sabūnas V, Radzijevskaja J, Sakalauskas P et al (2019) Dirofilaria repens in dogs and humans in Lithuania. Parasit Vectors 12:1–10. https://doi.org/10.1186/s13071-019-3406-y

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

    Article  CAS  Google Scholar 

  • Satjawongvanit H, Phumee A, Tiawsirisup S, et al (2019) Molecular analysis of canine filaria and its Wolbachia endosymbionts in domestic dogs collected from two animal university hospitals in Bangkok metropolitan region, Thailand. Pathogens 8:1–13. https://doi.org/10.3390/pathogens8030114

  • Senanayake MP, Infaq MLM, Adikaram SGS, Udagama PV (2013) Ocular and subcutaneous dirofilariasis in a Sri Lankan infant: an environmental hazard caused by dogs and mosquitoes. Paediatr Int Child Health 33:111–112. https://doi.org/10.1179/2046905512Y.0000000024

    Article  Google Scholar 

  • Sinhabahu VP, Hettiarachchi J, Gamage M, Beneragama DH (2018) A child with an unusual lump in the cheek. Sri Lanka J Child Heal 47:89–90. https://doi.org/10.4038/sljch.v47i1.8440

    Article  Google Scholar 

  • Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120

    Article  CAS  Google Scholar 

  • Tilakaratne WM, Pitakotuwage TN (2003) Intra-oral Dirofilaria repens infection: report of seven cases. J Oral Pathol Med 32:502–505. https://doi.org/10.1034/j.1600-0714.2003.00183.x

    Article  CAS  Google Scholar 

  • Traversa D, Aste G, Milillo P et al (2010) Autochthonous foci of canine and feline infections by Dirofilaria immitis and Dirofilaria repens in central Italy. Vet Parasitol 169:128–132. https://doi.org/10.1016/j.vetpar.2009.12.034

    Article  Google Scholar 

  • Vieira AL, Vieira MJ, Oliveira JM, et al (2014) Prevalence of canine heartworm (Dirofilaria immitis) disease in dogs of central Portugal. Parasite 21:1–7. https://doi.org/10.1051/parasite/2014003

  • Weerasekera CJ, Hapuachchige C, Wijeratne YMTY et al (2021) Omental dirofilariasis caused by Dirofilaria repens; visceralisation in a patient with diabetes mellitus. J Ceylon Coll Physicians 52:105. https://doi.org/10.4038/jccp.v52i2.7936

    Article  Google Scholar 

Download references

Acknowledgements

We thank Ms. A.H.M.W.S. Abeyrathne, at the Department of Veterinary Clinical Sciences, the University of Peradeniya, for assisting in collecting patient history.

Funding

This work was funded by the National Science Foundation (Grant No. RG/2019/BT/01) and National Research Council (Grant No. 20–083).

Author information

Authors and Affiliations

  1. Department of Parasitology, Faculty of Medicine, University of Ruhuna, Galle, Sri Lanka

    Sandani S. Thilakarathne

  2. Department of Zoology, Faculty of Science, University of Peradeniya, Peradeniya, 20400, Sri Lanka

    Sandani S. Thilakarathne, Piyumali K. Perera & Rupika S. Rajakaruna

  3. Department of Veterinary Clinical Sciences, Faculty of Veterinary Medicine and Animal Science, University of Peradeniya, Peradeniya, Sri Lanka

    Nayana Wijayawardhane & Chandima Mallawa

Authors
  1. Sandani S. Thilakarathne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nayana Wijayawardhane
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Piyumali K. Perera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chandima Mallawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rupika S. Rajakaruna
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Study conception and design by Rupika S. Rajakaruna and Nayana Wijayawardhane. Sample processing, data analysis, and writing of the manuscript by Sandani S. Thilakarathne. Supervision of laboratory work and data analysis by Piyumali K. Perera. Sample and patient history collection and laboratory assistance by Chandima Mallawa. All the authors critically edited and approved the final manuscript.

Corresponding author

Correspondence to Rupika S. Rajakaruna.

Ethics declarations

Ethical statement

Ethical clearance for the study was obtained from the Ethical Clearance Committee of the Postgraduate Institute of Science, University of Peradeniya, Sri Lanka. No: CES_PGIS_2022_06.

Consent to participate

N/A.

Consent for publication

All the authors read and approved the final version of the manuscript.

Conflict of interest

The authors declare no competing interests.

Additional information

Handling Editor: Una Ryan

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thilakarathne, S.S., Wijayawardhane, N., Perera, P.K. et al. Filariasis in dogs brought to the Veterinary Teaching Hospital, University of Peradeniya, Sri Lanka. Parasitol Res 122, 461–469 (2023). https://doi.org/10.1007/s00436-022-07742-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-022-07742-x

Keywords

Search

Navigation