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Parasitology Research

, Volume 117, Issue 5, pp 1581–1590 | Cite as

Longitudinal study for anthelmintic efficacy against intestinal helminths in naturally exposed Lithuanian village dogs: critical analysis of feasibility and limitations

  • Ž. Vienažindienė
  • D. E. Joekel
  • R. Schaper
  • P. Deplazes
  • M. Šarkūnas
Original Paper

Abstract

The efficacy of anthelmintic treatment at 1, 3, and 6 month intervals was evaluated in a prospective controlled field study with naturally exposed Lithuanian village dogs by monthly coproscopy during 1 year. A placebo-treated control group (C) (n = 202) and groups treated with two broad-spectrum anthelmintics, febantel/pyrantel-embonate/praziquantel (Drontal® Plus, Bayer) (D1, D3, D6; n = 113–117) and emodepside/praziquantel (Profender®, Bayer) (P1, P3, P6; n = 114–119), were included. At the beginning of the study, eggs of Toxocara canis (4.02%) and T. cati (0.44%) identified morphometrically and/or molecularly and eggs of taeniid- (0.78%) and Capillaria-like eggs (5.03%) were present in the feces without significant differences in prevalence between groups. Significant decreases in excretion of T. canis eggs was found 1 month after the treatment with Drontal® Plus in February (D1) and with Profender® in October (P1), November (P1), December (P3), February (P1), and March (P1, P3), as compared to controls in the same months. The incidence of egg excretion per dog at least once a year was significantly lower in group P1 for T. canis (4.24%; p < 0.01) and in groups D1, P1 for taeniid eggs (0%; p < 0.01 and p < 0.001), when compared to controls (16.96 and 6.70%, respectively). A critical analyses of factors possibly responsible for intestinal passage of canine helminth eggs revealed that chained dogs excreted T. canis eggs more frequently 1 month after treatment compared to dogs in pens, particularly from November to March (p = 0.01). The incidence of single detection of T. cati eggs was significantly increased in chained dogs (12.46%) as compared to fenced dogs (1.08%; p = 0.0001).

Keywords

Toxocara Anthelminthic treatment Field studies Coprophagia 

Notes

Acknowledgments

We acknowledge Edita Tamošiūnienė, Vilija Laurinavičiūtė, Giedrė Valauskaitė, Artūras Poderis, Indrė Ramanauskaitė, and Francesca Gori for valuable technical assistance during the study.

Funding

The study was supported by Bayer Animal Health GmbH, Leverkusen, Germany.

Compliance with ethical standards

Conflict of interest

Roland Schaper is an employee of Bayer Animal Health GmbH. The authors declare that they have no conflicts of interest.

Ethical standards

All applicable international and institutional guidelines for the care and use of animals were followed. The study was conducted in compliance with Lithuanian animal welfare regulations (No. B1-866, 2012; No. XI-2271, 2012).

References

  1. Altreuther G, Schimmel A, Schroeder I, Bach T, Charles S, Kok JD, Kraemes F, Wolken S, Young D, Krieges JK (2009) Efficacy of emodepside plus praziquantel tablets (Profender® tablets for dogs) against mature and immature infections with Toxocara canis and Toxascaris leonina in dogs. Parasitol Res 105:1–8CrossRefGoogle Scholar
  2. Barrs VR, Martin P, Nicoll RG, Beatty JA, Malik R (2000) Pulmonary cryptococcosis and Capillaria aerophila infection in an FIV-positive cat. Aust Vet J 78:154–158CrossRefPubMedGoogle Scholar
  3. Beveridge I, Rickard MD, Gregory GG, Munday BL (1975) Studies on Anoplotenia dayuri Beddard, 1911 (Cestoda: Taeniidae) a parasite of the Tasmanian devil: observations on the egg and metacestode. Int J Parasitol 5:251–267Google Scholar
  4. Bružinskaitė R, Šarkūnas M, Torgerson PR, Mathis A, Deplazes P (2009) Echinococcus in pigs and intestinal infection with Echinococcus spp. in dogs in southwestern Lithuania. Vet Parasitol 160:237–241CrossRefPubMedGoogle Scholar
  5. Burgess H, Ruotsalo K, Peregrine AS, Hanselman B, Abrams-Ogg A (2008) Eucoleus aerophilus respiratory infection in a dog with Addison's disease. Can Vet J 49:389–392PubMedPubMedCentralGoogle Scholar
  6. CAPC (Companion Animal Parasite Council) (2016) CAPC Recommendations. Intestinal Parasites (https://www.capcvet.org). Accessed 10/10/2017
  7. Coman BJ, Rickard MD (1975) The location of Taenia pisiformis, Taenia ovis and Taenia hydatigena in the gut of the dog and its effect on net environmental contamination with ova. Z Parasitenkd 47:237–248CrossRefPubMedGoogle Scholar
  8. Corsini M, Geissbühler U, Howard J, Gottstein B, Spreng D, Frey CF (2015) Clinical presentation, diagnosis, therapy and outcome of alveolar echinococcosis in dogs. Vet Rec 177:569.  https://doi.org/10.1136/vr.103470. PubMedGoogle Scholar
  9. Deplazes P, Eckert J (2001) Veterinary aspects of alveolar echinococcosis—a zoonosis of public health significance. Vet Parasitol 98:65–87CrossRefPubMedGoogle Scholar
  10. Deplazes P, Knapen F, Schweiger A, Overgaauw PAM (2011) Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis. Vet Parasitol 182:41–53CrossRefPubMedGoogle Scholar
  11. Deplazes P, Eckert J, Mathis A, von Samson-Himmelstjerna G, Zahner H (2016) Parasitology in veterinary medicine. Wageningen Academic Publishers, The NetherlandsGoogle Scholar
  12. Epe C, Schnieder T, Stoye M (1996) Opportunities and limitations of chemotherapeutic control of vertical infections of Toxocara canis and Ancylostoma caninum in the dog. Prakt Tierarzt 6:483–490Google Scholar
  13. ESCCAP (European Scientific Council Companion Animal Parasites) (2017). Guideline No. 1. Worm Control in Dogs and Cats (http://www.esccap.org/#1), 3rd edn. Accessed 17/09/2017
  14. Evinger JV, Kazacos KR, Cantwell HD (1985) Ivermectin for treatment of nasal capillariasis in a dog. J Am Vet Med Assoc 186:174–175PubMedGoogle Scholar
  15. Fahrion AS, Staebler S, Deplazes P (2008) Patent Toxocara canis infections in previously exposed and in helminth free dogs after infection with low numbers of embryonated eggs. Vet Parasitol 152:108–115CrossRefPubMedGoogle Scholar
  16. Fahrion AS, Schnyder M, Wichert B, Deplazes P (2011) Toxocara eggs shed by dogs and cats and their molecular and morphometric species-specific identification: is the finding of T. cati eggs shed by dogs of epidemiological relevance? Vet Parasitol 177:186–189.  https://doi.org/10.1016/j.vetpar.2010.11.028 CrossRefPubMedGoogle Scholar
  17. Greve JH, Tyler DE (1964) Cysticercus pisiformis (Cestoda: Taeniidae) in the liver of a dog. J Parasitol 50:712–716CrossRefPubMedGoogle Scholar
  18. Hopkins TJ (1991) Efficacy of a tablet containing pyrantel embonate, febantel and praziquantel against T. canis in dogs. Vet Rec 128:331CrossRefPubMedGoogle Scholar
  19. Hopkins TJ, Gyr P, Hedemann PM (1988) Nematocidal and cestocidal efficacy of a tablet formulation containing febantel, pyrantel emponate and praziquantel in dogs. Vet Med Rev 59:71–75Google Scholar
  20. Jacobs DE, Zhu X, Gasser RB, Chilton NB (1997) PCR-based methods for identification of potentially zoonotic ascaridoid parasites of the dog, fox and cat. Acta Trop 68:191–200CrossRefPubMedGoogle Scholar
  21. Jenkins DJ, Rickard WD (1985) Specific antibody responses to Taenia hydatigena, Taenia pisiformis and Echinococcus granulosus infection in dogs. Aust Vet J 623:72–78CrossRefGoogle Scholar
  22. Lloyd S, Gemmell MA (1992) Efficacy of a drug combination of praziquantel, pyrantel embonate, and febantel against helminth infections in dogs. Am J Vet Res 53:2272–2273PubMedGoogle Scholar
  23. Marcinkutė A, Šarkūnas M, Moks E, Saarma U, Jokelainen P, Bagrade B, Laivacuma S, Strupas K, Sokolovas S, Deplazes P (2015) Echinococcus infections in the Baltic region. Vet Parasitol 213:121–131CrossRefPubMedGoogle Scholar
  24. Mathis A, Deplazes P, Eckert J (1996) An improved test system for PCR-based specific detection of Echinococcus multilocularis eggs. J Helminthol 70:219–222CrossRefPubMedGoogle Scholar
  25. Miro G, Mateo M, Montoya A, Vela E, Calonge R (2007) Survey of intestinal parasites in stray dogs in the Madrid area and comparison of the efficacy of three anthelmintics in naturally infected dogs. Parasitol Res 100:317–320CrossRefPubMedGoogle Scholar
  26. Nagy A, Ziadinov I, Schweiger A, Schnyder M, Deplazes P (2011) Hair coat contamination with zoonotic helminth eggs of farm and pet dogs and foxes. Berl Munch Tierarztl Wochenschr 124:503–511PubMedGoogle Scholar
  27. Nijsse R, Mughini-Gras L, Wagenaar JA, Ploeger HW (2014) Coprophagy in dogs interferes in the diagnosis of parasitic infections by fecal examination. Vet Parasitol 204:304–309.  https://doi.org/10.1016/j.vetpar.2014.05.019 CrossRefPubMedGoogle Scholar
  28. Pezzullo JC (2009) StatPages.net. http://statpages.org/confint.html.
  29. Rijpstra AC, Smit AM, Swellengrebel NH (1961) How and where to search for the ova of Taenia saginata. Trop Geogr Med 13:160–166PubMedGoogle Scholar
  30. Rinaldi L, Pennacchio S, Musella V, Maurelli MP, La Torre F, Cringoli G (2015) Helminths control in kennels: is the combination of milbemycin oxime and praziquantel a right choise? Parasit Vectors 8:30.  https://doi.org/10.1186/s13071-015-0647-2 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Sager H, Moret C, Grimm F, Deplazes P, Doherr MG, Gottstein B (2006) Coprological study on intestinal helminths in Swiss dogs: temporal aspects of anthelminthic treatment. Parasitol Res 98:333–338CrossRefPubMedGoogle Scholar
  32. Schimmel A, Altreuther G, Schroeder I, Charles S, Cruthers L, Ketzis J, Kok DJ, Kraemer F, McCall JW, Krieger KJ (2009a) Efficacy of emodepside plus praziquantel tablets (Profender® tablets for dogs) against mature and immature adult Ancylostoma caninum and Uncinaria stenocephala infections in dogs. Parasitol Res 1051:9–16CrossRefGoogle Scholar
  33. Schimmel A, Altreuther G, Schroeder I, Charles S, Cruthers L, Kok DJ, Kraemer F, Krieger KJ (2009b) Efficacy of emodepside plus praziquantel tablets (Profender® tablets for dogs) against mature and immature adult Trichuris vulpis infections in dogs. Parasitol Res 1051:17–22CrossRefGoogle Scholar
  34. Schroeder I, Altreuter G, Schimmel A, Deplazes P, Kok DJ, Schnyder M, Krieger KJ (2009) Efficacy of emodepside plus praziquantel tablets (Profender® tablets for dogs) against mature and immature cestode infections in dogs. Parasitol Res 105:S1–S8CrossRefPubMedGoogle Scholar
  35. Silverman PH (1954) Studies on the biology of some tapeworms of the genus Taenia. 1. Factors affecting hatching and activation of taeniid ova and some criteria of their viability. Ann Trop Med Parasitol 48:207–215CrossRefPubMedGoogle Scholar
  36. Štefanić S, Shaikenov BS, Deplazes P, Dinkel A, Torgerson PR, Mathis A (2004) Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (“sheep strain”) in naturally infected dogs. Parasitol Res 92:347–351CrossRefPubMedGoogle Scholar
  37. Trachsel D, Deplazes P, Mathis A (2007) Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134:911–920CrossRefPubMedGoogle Scholar
  38. Traversa D, Cesare AD, Giulio ED, Castagna G, Schaper R, Braun G, Lohr B, Pampurini F, Milillo P, Strube K (2012) Efficacy and safety of imidacloprid 10%/moxidectin 1% spot-on formulation in the treatment of feline infection by Capillaria aerophila. Parasitol Res 111:1793–1798CrossRefPubMedPubMedCentralGoogle Scholar
  39. Uga S, Matsuo J, Kimura D, Rai SK, Koshino Y, Igarashi K (2000) Differentiation of Toxocara canis and T. cati eggs by light and scanning electron microscopy. Vet Parasitol 92:287–294CrossRefPubMedGoogle Scholar
  40. Van der Borg JAM, Graat EAM (2006) Pilot study to identify risk factors for coprophagic behaviour in dogs. In: De Meester R, Moons C, Mulkens F (eds). Proceedings of the VDWE International Congress on Companion Animal Behaviour and Welfare. Vlaamse Dierenartsenvereniging vzwGoogle Scholar
  41. Voge M, Berntzen AK (1963) Asexual multiplication of larval tapeworms as the cause of fatal parasitic ascites in dogs. J Parasitol 49:983–988CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ž. Vienažindienė
    • 1
  • D. E. Joekel
    • 2
  • R. Schaper
    • 3
  • P. Deplazes
    • 2
  • M. Šarkūnas
    • 1
  1. 1.Department of Veterinary Pathobiology, Veterinary AcademyLithuanian University of Health SciencesKaunasLithuania
  2. 2.Institute of ParasitologyUniversity of ZurichZurichSwitzerland
  3. 3.Bayer Animal Health GmbHVeterinary Scientific AffairsLeverkusenGermany

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