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Anthelmintic tolerance in free-living and facultative parasitic isolates of Halicephalobus (Panagrolaimidae)

Published online by Cambridge University Press:  13 April 2012

P. FONDERIE*
Affiliation:
Nematology Unit, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium
W. BERT
Affiliation:
Nematology Unit, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium
F. HENDRICKX
Affiliation:
Terrestrial Ecology Unit, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium Royal Belgian Institute of Natural Sciences, rue Vautiers 29, 1000 Brussels, Belgium
W. HOUTHOOFD
Affiliation:
Nematology Unit, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium
T. MOENS
Affiliation:
Marine Biology Section, Department of Biology, Ghent University, Krijgslaan 281 S8, 9000 Ghent, Belgium
*
*Corresponding author: Nematology Unit, Department of Biology, Ghent University; K.L. Ledeganckstraat 35, 9000 Ghent, Belgium. Tel: +32 92645225. Fax: +32 92645344. E-mail: [email protected]

Summary

Studies on anthelmintic resistance in equine parasites do not include facultative parasites. Halicephalobus gingivalis is a free-living bacterivorous nematode and a known facultative parasite of horses with a strong indication of some form of tolerance to common anthelmintic drugs. This research presents the results of an in vitro study on the anthelmintic tolerance of several isolates of Halicephalobus to thiabendazole and ivermectin using an adaptation of the Micro-Agar Larval Development Test hereby focusing on egg hatching and larval development. Panagrellus redivivus and Panagrolaimus superbus were included as a positive control. The results generally show that the anthelmintic tolerance of Halicephalobus to both thiabendazole and ivermectin was considerably higher than that of the closely related Panagrolaimidae and, compared to other studies, than that of obligatory equine parasites. Our results further reveal a remarkable trend of increasing tolerance from fully free-living isolates towards horse-associated isolates. In vitro anthelmintic testing with free-living and facultative parasitic nematodes offers the advantage of observing drug effect on the complete life cycle as opposed to obligatory parasites that can only be followed until the third larval stage. We therefore propose Halicephalobus gingivalis as an experimental tool to deepen our understanding of the biology of anthelmintic tolerance.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Agresti, A. (2002). Categorical Data Analysis 2nd Edn. Wiley-Interscience, New Jersey, USA.CrossRefGoogle Scholar
Akagami, M., Shibahara, T., Yoshiga, T., Tanak, N., Yaguchi, Y., Onuki, T., Kondo, T., Yamanaka, T., and Kubo, M. (2007). Granulomatous nephritis and meningoencephalomyelitis caused by Halicephalobus gingivalis in a pony gelding. Journal of Veterinary Medical Science 69, 11871190.CrossRefGoogle Scholar
Anderson, R. C., Linder, K. E. and Peregrine, A. S. (1998). Halicephalobus gingivalis (Stefansky, 1954) from a fatal infection in a horse in Ontario, Canada with comments on the validity of H. gingivalis and a review of the genus. Parasite 5, 255261.CrossRefGoogle Scholar
Andrássy, I. (1984). Klasse Nematoda (Ordnungen Monhysterida, Desmoscolecida, Araeolaimidae, Chromadorida, Rhabditida). Gustav Fischer Verlag, Stuttgart, Germany.CrossRefGoogle Scholar
Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. and Wheeler, D. (2008). GenBank. Nucleic Acids Research 36, D25-D30. doi: 10.1093/nar/gkm929 CrossRefGoogle ScholarPubMed
Blunden, A. S., Khalil, L. F. and Webbon, P. M. (1987). Halicephalobus deletrix infection in a horse. Equine Veterinary Journal 19, 255260.CrossRefGoogle ScholarPubMed
Boswinkel, M., Neyens, I. J. S. and Sloet van Oldruitenborgh-Oosterbaan, M. M. (2006). Halicephalobus gingivalis infection in a 5-year old Tinker gelding. Tijdschrift voor Diergeneeskunde 131, 7480.Google Scholar
Brady, H. A. and Nichols, W. T. (2009). Drug resistance in equine parasites: an emerging global problem. Journal of Equine Veterinary Science 29, 285295.CrossRefGoogle Scholar
Brenner, S. (1974). The genetics of Caenorhabditis elegans . Genetics 77, 7194.CrossRefGoogle ScholarPubMed
Coles, G. C. (2006). Drug resistance or drug tolerance in parasites. Trends in Parasitology 22, 348.CrossRefGoogle ScholarPubMed
Coles, G. C., Jackson, F., Pomroy, W. E., Prichard, R. K., von Samson-Himmelstjerna, G., Silvestre, A., Taylor, M. A. and Vercruysse, J. (2006). The detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology 136, 167185.CrossRefGoogle ScholarPubMed
Dunn, D. G., Gardiner, C. H., Dralle, K. R. and Thilsted, J. P. (1993). Nodular granulomatous posthitis caused by Halicephalobus (syn. Micronema) sp. in a horse. Veterinary Pathology 30, 586589.CrossRefGoogle ScholarPubMed
Elsworth, B., Wasmuth, J. and Blaxter, M. (2011). NEMBASE4: The nematode transcriptome resource. International Journal for Parasitology 41, 881894.CrossRefGoogle ScholarPubMed
Fallon, P. G., Tao, L. F., Ismail, M. M. and Bennett, J. L. (1996). Schistosome resistance to praziquantel: Fact or artifact? Parasitology Today 12, 316320.CrossRefGoogle ScholarPubMed
Ferguson, R., van Dreumel, T., Keystone, J. S., Manning, A., Malatestinic, A., Caswell, J. L. and Peregrine, A. S. (2008). Unsuccessful treatment of a horse with mandibular graulomatous osteomyelitis due to Halicephalobus gingivalis . Canadian Veterinary Journal 49, 10991103.Google Scholar
Fonderie, P., Willems, M., Bert, W., Houthoofd, W., Steel, H., Claeys, M. and Borgonie, G. (2009). Intestine ultrastructure of the facultative parasite Halicephalobus gingivalis (Nematoda: Panagrolaimidae). Nematology 11, 859868.CrossRefGoogle Scholar
Geary, T. G. and Thompson, D. P. (2001). Caenorhabditis elegans: How good a model for veterinary parasites? Veterinary Parasitology 101, 371386.CrossRefGoogle Scholar
Geraert, E., Sudhaus, W., Lenaerts, L. and Bosmans, E. (1988). Halicephalobus laticauda sp. n., a nematode found in a Belgian coal mine (Nematoda, Rhabditida). Annales de la Société Royale Zoologique de Belgique 118, 512.Google Scholar
Gokbulut, C., Cirak, V. Y., Senlik, B., Aksit, D., Durmaz, M. and McKellar, Q. A. (2010). Comparative plasma disposition, bioavailability and efficacy of ivermectin following oral and pour-on administrations in horses. Veterinary Parasitology 170, 120126.CrossRefGoogle ScholarPubMed
Holden-Dye, L. and Walker, R. J. (2007).Anthelmintic drugs In WormBook (ed. The C. elegans Research Community, WormBook) doi/10.1895/wormbook.1.7.1, http://www.wormbook.org.Google Scholar
Isaza, R., Schiller, C. A., Stover, J., Smith, P. J. and Greiner, E. C. (2000). Halicephalobus gingivalis (Nematoda) infection in a Grevy's zebra (Equis grevyi). Journal of Zoo and Wildlife Medicine 31, 7781.Google Scholar
James, C. E. and Davey, M. W. (2009). Increased expression of ABC transport proteins is associated with ivermectin resistance in the model nematode Caenorhabditis elegans . International Journal for Parasitology 39, 213220.CrossRefGoogle ScholarPubMed
James, C. E., Hudson, A. L. and Davey, M. W. (2009). Drug resistance mechanisms in helminths: is it survival of the fittest? Trends in Parasitology 25, 328335.CrossRefGoogle ScholarPubMed
Johnson, J. S., Hibler, C. P., Tillotson, K. M. and Mason, G. L. (2001). Radiculomeningomyelitis due to Halicephalobus gingivalis in a horse. Veterinary Pathology 38, 559561.CrossRefGoogle ScholarPubMed
Kenward, M. G. and Roger, J. H. (1997). Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53, 983997.CrossRefGoogle ScholarPubMed
Lacey, E., Redwin, J. M., Gill, G. H., Demargheriti, V. M. and Waller, P. J. (1991). A larval development assay for the simultaneous detection of broad spectrum anthelmintic resistance. In Resistance of Parasites to Anti-parasitic Drugs (ed. Boray, J. C., Martin, P. J. and Roush, R. T.), pp. 177184. MSD AGVET, Rahway, New Jersey, USA.Google Scholar
Min, B. R. and Hart, S. P. (2003). Tannins for suppression of internal parasites. Journal of Animal Science 81, E102E109.Google Scholar
Müller, S., Grzybowski, M., Sager, H., Bornand, V. and Brehm, W. (2008). A nodular granulomatous posthitis caused by Halicephalobus sp. in a horse. Veterinary Dermatology 19, 4448.CrossRefGoogle ScholarPubMed
Nadler, S. A., Carreno, R. A., Adams, B. J., Kinde, H., Baldwin, J. G. and Mundo-Ocampo, M. (2003). Molecular genetics and diagnosis of soil and clinical isolates of Halicephalobus gingivalis (Nematoda: Cephalobina: Panagrolaimoidea), an opportunistic pathogen of horses. International Journal for Parasitology 33, 11151125.CrossRefGoogle ScholarPubMed
Ondrejka, S. L., Procop, G. W., Lai, K. K. and Prayson, R. A. (2010). Fatal parasitic meningoencephalomyelitis caused by Halicephalobus deletrix. A case report and review of the literature. Archives of Pathology and Laboratory Medicine 134, 625629.CrossRefGoogle ScholarPubMed
Patel, M. R. (1997). Effects of ivermectin on eggs and first-stage larvae of nematodes. Bios 68, 152162.Google Scholar
Pearce, S. G., Bouré, L. P., Taylor, J. A. and Peregrine, A. S. (2001). Treatment of a granuloma caused by Halicephalobus gingivalis in a horse. Journal of the American Veterinary Medical Association 219, 17351738.CrossRefGoogle ScholarPubMed
Rames, D. S., Miller, D. K., Barthel, R., Craig, T. M., Dziezyc, J., Helman, R. G. and Mealey, R. (1995). Ocular Halicephalobus (syn. Micronema) deletrix in a horse. Veterinary Pathology 32, 540542.CrossRefGoogle ScholarPubMed
Sangster, N. C., Batterham, P., Chapman, H. D., Duraisingh, M., Le Jambre, L., Shirley, M., Upcroft, J. and Upcroft, P. (2002). Resistance to antiparasitic drugs: the role of molecular diagnosis. International Journal for Parasitology 32, 637653.CrossRefGoogle ScholarPubMed
Shokoohi, E., Abolafia, J. and Zad, J. (2007). Nematodes of the order Rhabditida from Tehran province, Iran. The family Panagrolaimidae with description of Halicephalobus persicus sp. n. and a key to species of Halicephalobus Timm, 1956. Nematology 9, 693711.CrossRefGoogle Scholar
Simpkin, K. G. and Coles, G. C. (1980). The use of Caenorhabditis elegans for anthelmintic screening. Journal of Chemical Technology and BioTechnology 31, 6669.Google Scholar
Spalding, M. G., Greiner, E. C. and Green, S. L. (1990). Halicephalobus (Micronema) deletrix infection in two half-sibling foals. Journal of the American Veterinary Medical Association 196, 11271129.CrossRefGoogle ScholarPubMed
Steel, H., de la Peña, E., Fonderie, P., Willekens, K., Borgonie, G. and Bert, W. (2010). Nematode succession during composting and the potential of the nematode community as an indicator of compost maturity. Pedobiologia 53, 181190.CrossRefGoogle Scholar
Stefansky, W. (1954). Rhabditis gingivalis sp. n. parasite trouvé dans un granulome de la gencive chez un cheval. Acta Parasitologica 1, 329334.Google Scholar
Taylor, M. A., Hunt, K. R. and Goodyear, K. L. (2002). Anthelmintic resistance detection methods. Veterinary Parasitology 103, 183194.CrossRefGoogle ScholarPubMed
Ura, K., Kai, T., Sakata, S., Iguchi, T. and Arizono, K. (2002). Aquatic acute toxicity testing using the nematode Caenorhabditis elegans . Journal of Health Science 48, 583586.CrossRefGoogle Scholar
Várady, M., Čorba, J., Letková, V. and Kováč, G. (2009). Comparison of two versions of larval development test to detect anthelmintic resistance in Haemonchus contortus . Veterinary Parasitology 160, 267271.CrossRefGoogle ScholarPubMed