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Hammondia triffittae n. comb. of foxes (Vulpes spp.): biological and molecular characteristics and differentiation from Hammondia heydorni of dogs

Published online by Cambridge University Press:  21 September 2010

BJØRN GJERDE  and
STINA S. DAHLGREN
BJØRN GJERDE*
Affiliation:
Norwegian School of Veterinary Science, Department of Food Safety and Infection Biology, Section of Microbiology, Immunology and Parasitology, P.O. Box 8146 Dep., 0033 Oslo, Norway
STINA S. DAHLGREN
Affiliation:
Norwegian School of Veterinary Science, Department of Food Safety and Infection Biology, Section of Microbiology, Immunology and Parasitology, P.O. Box 8146 Dep., 0033 Oslo, Norway
*
*Corresponding author: Tel: +47 22 96 49 64. Fax: +47 22 96 49 65. E-mail: Bjorn.Gjerde@nvh.no
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Summary

Genomic DNAs from 3 oocyst isolates of Hammondia sp. from foxes (Vulpes vulpes and V. lagopus) and 1 oocyst isolate of Hammondia heydorni from a dog, were examined by PCR and sequence analysis of 6 loci in order to determine whether the isolates were conspecific. Consistent genetic differences were found between the fox and dog isolates, respectively, at the ITS-2 region, the lsu rRNA gene, the alpha tubulin gene and the HSP70 gene, but not at the ssu rRNA gene or ITS-1 locus. Infection experiments established that dogs were unsuitable as definitive hosts for Hammondia sp. of foxes; hence this species is regarded as separate from H. heydorni of wolf-like canids, but probably identical with Isospora triffittae (syn. Isospora triffitti) previously reported from foxes. This species has therefore been named Hammondia triffittae n. comb. Reindeer, moose, sheep, goats, foxes and rabbits may act as intermediate hosts for H. triffittae. Muscle tissues of inoculated intermediate hosts were infectious for foxes from 16 days post-infection. Oocysts of H. triffittae were subspherical, averaging 12·5×10·9 μm in size. The lsu rRNA gene and the alpha tubulin gene seem to be suitable genetic markers for differentiating between H. triffittae and H. heydorni.

Keywords

Hammondia triffittaeHammondia heydornifoxesdogslife cyclemolecular characterization
Type
Research Article
Information
Parasitology , Volume 138 , Issue 3 , March 2011 , pp. 303 - 321
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Abel, J., Schares, G., Orzeszko, K., Gasser, R. B. and Ellis, J. T. (2006). Hammondia isolated from dogs and foxes are genetically distinct. Parasitology 132, 187–192. doi: 10.1017/S0031182005008814.CrossRefGoogle ScholarPubMed
Ashford, R. W. (1977). The fox, Vulpes vulpes, as a final host for Sarcocystis of sheep. Annals of Tropical Medicine and Parasitology 71, 29–34.CrossRefGoogle ScholarPubMed
Bardeleben, C., Moore, R. L. and Wayne, R. K. (2005). A molecular phylogeny of the Canidae based on six nuclear loci. Molecular Phylogenetics and Evolution 37, 815–831. doi: 10.1016/j.ympev.2005.07.019.CrossRefGoogle ScholarPubMed
Barratt, J., Al-Qassab, S., Reichel, M. P. and Ellis, J. T. (2008). The development and evaluation of a nested PCR assay for detection of Neospora caninum and Hammondia heydorni in feral mouse tissues. Molecular and Cellular Probes 22, 228–233. doi: 10.1016/j.mcp.2008.03.001.CrossRefGoogle ScholarPubMed
Dahlgren, S. S. and Gjerde, B. (2007). Genetic characterization of six Sarcocystis species from reindeer (Rangifer tarandus tarandus) in Norway based on the small subunit rRNA gene. Veterinary Parasitology 146, 204–213. doi: 10.1016/j.vetpar.2007.02.023.CrossRefGoogle ScholarPubMed
Dahlgren, S. S. and Gjerde, B. (2010). The red fox (Vulpes vulpes) and the arctic fox (Vulpes lagopus) are definitive hosts of Sarcocystis alces and Sarcocystis hjorti from moose (Alces alces). Parasitology 137, 1547–1557. doi: 10.1017/S0031182010000399.CrossRefGoogle ScholarPubMed
Dissanaike, A. S. and Kan, S. P. (1977). Isospora heydorni-type oocysts in faeces of a dog. Asian Journal of Tropical Medicine and Public Health 8, 419.Google ScholarPubMed
Dubey, J. P. (1977). Toxoplasma, Hammondia, Besnoitia, Sarcocystis, and other tissue cyst-forming coccidia of man and animals. In Parasitic Protozoa (ed. Krier, J. P.), pp. 101–237. Academic Press, New York, USA.Google Scholar
Dubey, J. P. (1982). Sarcocystis and other coccidia in foxes and other wild carnivores from Montana. Journal of the American Veterinary Medical Association 181, 1270–1271.Google ScholarPubMed
Dubey, J. P. and Fayer, R. (1976). Development of Isospora bigemina in dogs and other mammals. Parasitology 73, 371–380. doi: 10.1017/S0031182000047041.CrossRefGoogle ScholarPubMed
Dubey, J. P., Sreekumar, C., Miska, K. B., Hill, D. E., Vianna, M. C. B. and Lindsay, D. S. (2004). Molecular and biological characterization of Hammondia heydorni-like oocysts from a dog fed hearts from naturally infected white-tailed deer (Odocoileus virginianus). Journal of Parasitology 90, 1174–1176. doi: 10.1645/GE-324R.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Williams, C. S. F. (1980). Hammondia heydorni infection in sheep, goats, moose, dogs and coyotes. Parasitology 81, 123–127. doi: 10.1017/S0031182000055098.CrossRefGoogle ScholarPubMed
Ellis, J. T., Morrison, D. A., Liddell, S., Jenkins, M., Mohammed, O. B., Ryce, C. and Dubey, J. P. (1999). The genus Hammondia is paraphyletic. Parasitology 118, 357–362. doi:10.1017/S0031182098003801.CrossRefGoogle ScholarPubMed
Entzeroth, R., Scholtyseck, E. and Greuel, E. (1978). The roe deer intermediate host of different coccidia. Naturwissenschaften 65, 395.CrossRefGoogle ScholarPubMed
Fayer, R. (1974). Development of Sarcocystis fusiformis in the small intestines of the dog. Journal of Parasitology 60, 660–665.CrossRefGoogle ScholarPubMed
Frenkel, J. K. and Dubey, J. P. (1975). Hammondia hammondi gen. nov., sp. nov., from domestic cats, a new coccidian related to Toxoplasma and Sarcocystis. Zeitschrift für Parasitenkunde 46, 3–12.CrossRefGoogle ScholarPubMed
Gerasimchik, V. A. (2005). [The parasite fauna of silver-black foxes (Vulpes fulvus) on fur farms of the Republic of Belarus.] [The Proceedings of the National Academy of Sciences of Belarus. Series of Agrarian Sciences] 3, 79–83. [In Russian.]Google Scholar
Gerasimchik, V. A. (2006). [Epizootology of isosporosis and nematodosis of polar foxes in the fur farms of the Republic of Belarus.] [Epizootiology, Immunology, Pharmacology and Sanitation] 1, 7–10. [In Russian.]Google Scholar
Gjerde, B. (1983). Shedding of Hammondia heydorni-like oocysts by foxes fed muscular tissue of reindeer (Rangifer tarandus). Acta Veterinaria Scandinavica 24, 241–243.CrossRefGoogle ScholarPubMed
Gjerde, B. and Bjerkås, I. (1987). Intestinal development of a Hammondia heydorni-like parasite in experimentally infected foxes. [Abstracts presented at the annual meeting and symposium of the Nordic Association for Veterinary Pathology (NFVP), in Helsinki, Finland, June 11–12, 1987.] Suomen Eläinlääkärilehti 93, 7–8.Google Scholar
Gjerde, B. and Helle, O. (1982). Rein som mellomvert for Sarcocystis spp. og Hammondia sp. Norsk Veterinærtidsskrift 94, 663–664.Google Scholar
Golemanski, V. and Ridzhakov, N. (1975). V'rkho koktsidiite (Protozoa, Coccidia) na lisitsite v B'lgariya. [On coccidia (Protozoa, Coccidia) in the foxes in Bulgaria.] Acta Zoologica Bulgarica 3, 3–18. [In Russian.]Google Scholar
Graphodatsky, A. S., Perelman, P. L., Sokolovskaya, N. V., Beklemisheva, V. R., Serdukova, N. A., Dobigny, G., O'Brien, S. J., Ferguson-Smith, M. A. and Yang, F. (2008). Phylogenomics of the dog and fox family (Canidae, Carnivora) revealed by chromosome painting. Chromosome Research 16, 129–143. doi: 10.1007/s10577-007-1203-5.CrossRefGoogle ScholarPubMed
Heydorn, A. O. (1973). Zum Lebenszyklus der kleinen Form von Isospora bigemina des Hundes. 1. Rind und Hund als mögliche Zwischenwirte. Berliner und Münchener Tierärztliche Wochenschrift 86, 323–329.Google Scholar
Heydorn, A. O., Gestrich, R. and Ipczynski, V. (1975). Zum lebenszyklus der kleinen Form von Isospora bigemina des Hundes. II. Entwicklungsstadien im Darm des Hundes. Berliner und Münchener Tierärztliche Wochenschrift 88, 449–453.Google Scholar
Jenkins, M. C., Ellis, J. T., Liddell, S., Ryce, C., Munday, B. L., Morrison, D. A. and Dubey, J. P. (1999). The relationship of Hammondia hammondi and Sarcocystis mucosa to other heteroxenous cyst-forming coccidia as inferred by phylogenetic analysis of the 18S SSU ribosomal DNA sequence. Parasitology 119, 135–142. doi: 10.1017/S0031182099004618.CrossRefGoogle ScholarPubMed
Lee, C. D. (1934). The pathology of coccidiosis in the dog. (1934). Journal of the American Veterinary Medical Association 85, 760–781.Google Scholar
Levine, N. D. (1985). Erhardorina n. g., Ascogregarina polynesiensis n. sp., Eimeria golemanskii n. sp., Isospora tamariscini n. sp., Gregarina kazumii n. nom., new combinations and emendations in the names of apicomplexan protozoa. Journal of Protozoology 32, 359–363. doi: 10.1111/j.1550-7408.1985.tb03068.x.CrossRefGoogle Scholar
Margolin, J. H. and Jolley, W. R. (1979). Experimental infection of dogs with Sarcocystis from wapiti. Journal of Wildlife Diseases 15, 259–262.CrossRefGoogle ScholarPubMed
Marsh, A. E., Barr, B. C., Packham, A. E. and Conrad, P. A. (1998). Description of a new Neospora species (Protozoa: Apicomplexa: Sarcocystidae). Journal of Parasitology 84, 983–891.CrossRefGoogle ScholarPubMed
Marsh, A. E., Howe, D. K., Wang, G., Barr, B. C., Cannon, N. and Conrad, P. A. (1999). Differentiation of Neospora hughesi from Neospora caninum based on their immunodominant surface antigen, SAG1 and SRS2. International Journal for Parasitology 29, 1575–1582. doi: 10.1016/S0020-7519(99)00120-4.CrossRefGoogle ScholarPubMed
Matsui, T. (1991). The tissue stages of Isospora heydorni in the guinea pig as an intermediate host. Japanese Journal of Parasitology 40, 581–586.Google Scholar
Matsui, T., Morii, T., Iijima, T., Ito, S., Tsunoda, K., Correa, W. M. and Fujino, T. (1981). Cyclic transmission of the small type of Isospora bigemina of the dog. Japanese Journal of Parasitology 30, 179–186.Google Scholar
McAllister, M. M., Dubey, J. P., Lindsay, D. S., Jolley, W. R., Wills, R. A. and McGuire, A. M. (1998). Dogs are definitive hosts of Neospora caninum. International Journal for Parasitology 28, 1473–1478.CrossRefGoogle ScholarPubMed
Mohammed, O. B., Davies, A., Hussein, H. S., Daszak, P. and Ellis, J. T. (2003). Hammondia heydorni from the Arabian mountain gazelle and red fox in Saudi Arabia. Journal of Parasitology 89, 535–539. doi: 10.1645/0022-3395(2003)089.CrossRefGoogle ScholarPubMed
Monteiro, R. M., Richtzenhain, L. J., Pena, H. F., Souza, S. L., Funada, M. R., Gennari, S. M., Dubey, J. P., Sreekumar, C., Keid, L. B. and Soares, R. M. (2007). Molecular phylogenetic analysis in Hammondia-like organisms based on partial Hsp70 coding sequences. Parasitology 134, 1195–1203. doi: 10.1017/S0031182007002612.CrossRefGoogle ScholarPubMed
Morrison, D. A., Bornstein, S., Thebo, P., Wernery, U., Kinne, J. and Mattsson, J. G. (2004). The current status of the small subunit rRNA phylogeny of the coccidia (Sporozoa). International Journal for Parasitology 34, 501–514. doi: 10.1016/j.ijpara.2003.11.006.CrossRefGoogle ScholarPubMed
Nassar, A. M., Hilali, M. and Rommel, M. (1983). Hammondia heydorni infection in camels (Camelus dromedarius) and water buffaloes (Bubalus bubalus) in Egypt. Zeitschrift für Parasitenkunde 69, 693–694.CrossRefGoogle ScholarPubMed
Nukerbaeva, K. K. and Svanbaev, S. K. (1973). Koktsidii pushnykh zverei v Kazakhstane. [Coccidia of fur-bearing mammals in Kazakhstan]. Vestnik Sel'skokhozyaistvennoi Nauki Kazakhstana 12, 50–54.Google Scholar
Payne, S. and Ellis, J. T. (1996). Detection of Neospora caninum DNA by the polymerase chain reaction. International Journal for Parasitology 26, 347–351.CrossRefGoogle ScholarPubMed
Schares, G., Heydorn, A. O., Cüppers, A., Mehlhorn, H., Geue, L., Peters, M. and Conraths, F. J. (2002). In contrast to dogs, red foxes (Vulpes vulpes) did not shed Neospora caninum upon feeding intermediate host tissues. Parasitology Research 88, 44–52. doi: 10.1007/s004360100496.CrossRefGoogle Scholar
Schares, G., Meyer, J., Bärwald, A., Conraths, F. J., Riebe, R., Bohne, W., Rohn, K. and Peters, M. (2003). A Hammondia-like parasite from the European fox (Vulpes vulpes) forms biologically viable tissue cysts in cell culture. International Journal for Parasitology 33, 229–234. doi: 10.1016/S0020-7519(03)00009-2.CrossRefGoogle ScholarPubMed
Siverajah, S., Ryce, C., Morrison, D. A. and Ellis, J. T. (2003). Characterization of an alpha tubulin gene sequence from Neospora caninum and Hammondia heydorni, and their comparison to homologous genes from Apicomplexa. Parasitology 126, 561–569. doi: 10.1017/S0031182003003135.Google ScholarPubMed
Šlapeta, J. R., Koudela, B., Votýpka, J., Modrý, D., Hořejš, R. and Lukeš, J. (2002 a). Coprodiagnosis of Hammondia heydorni in dogs by PCR based amplification of ITS 1 rRNA: differentiation from morphologically indistinguishable oocysts of Neospora caninum. The Veterinary Journal 163, 147–154. doi: 10.1053/tvjl.2001.0599.CrossRefGoogle ScholarPubMed
Šlapeta, J. R., Modrý, D., Kyselová, I., Hořejš, R., Lukeš, J. and Koudela, B. (2002 b). Dog shedding oocysts of Neospora caninum: PCR diagnosis and molecular phylogenetic approach. Veterinary Parasitology 109, 157–167. doi: 10.1016/S0304-4017(02)00273-X.CrossRefGoogle ScholarPubMed
Šlapeta, J. R., Modrý, D., Votýpka, J., Jirků, M., Lukeš, J. and Koudela, B. (2003). Evolutionary relationships among cyst-forming coccidia Sarcocystis spp. (Alveolata: Apicomplexa: Coccidea) in endemic African tree vipers and perspective for evolution of heteroxenous life cycle. Molecular Phylogenetics and Evolution 27, 464–475. doi: 10.1016/S1055-7903(03)-00018-6.CrossRefGoogle ScholarPubMed
Soares, R. M., Cortez, L. R., Gennari, S. M., Sercundes, M. K., Keid, L. B. and Pena, H. F. (2009). Crab-eating fox (Cerdocyon thous), a South American canid, as a definitive host for Hammondia heydorni. Veterinary Parasitology 162, 46–50. doi: 10.1016/j.vetpar.2009.02.003.CrossRefGoogle ScholarPubMed
Su, C., Evans, D., Cole, R. H., Kissinger, J. C., Ajioka, J. W. and Sibley, L. D. (2003). Recent expansion of Toxoplasma through enhanced oral transmission. Science 299, 414–416. doi: 10.1126/science.1078035.CrossRefGoogle ScholarPubMed
Tadros, W. and Laarman, J. J. (1976). Sarcocystis and related coccidian parasites: A brief general review, together with a discussion on some biological aspects of their life cycles and a new proposal for their classification. Acta Leidensia 44, 1–107.Google Scholar
Triffitt, M. J. (1927). Observations on the oocysts of coccidia found in the faeces of carnivores. Protozoology 3, 65–74. [Supplement to Journal of Helminthology.]Google Scholar
Walsh, C. P., Vemulapalli, R., Sriranganathan, N., Zajac, A. M., Jenkins, M. C. and Lindsay, D. S. (2001). Molecular comparison of the dense granule proteins GRA6 and GRA7 of Neospora hughesi and Neospora caninum. International Journal for Parasitology 31, 253–358. doi: 10.1016/S0020-7519(00)00169-7.CrossRefGoogle ScholarPubMed
Wapenaar, W., Jenkins, M. C., O'Handley, R. M. and Barkema, H. W. (2006). Neospora caninum-like oocysts observed in feces of free-ranging red foxes (Vulpes vulpes) and coyotes (Canis latrans). Journal of Parasitology 92, 270–1274. doi: 10.1645/GE-913R.1.CrossRefGoogle ScholarPubMed
Warrag, M. and Hussein, H. S. (1983). The camel (Camelus dromedarius) as an intermediate host for Hammondia heydorni. Journal of Parasitology 69, 926–929.CrossRefGoogle ScholarPubMed
Wenyon, C. M. (1926). Coccidia of the genus Isospora in cats, dogs and man. Parasitology 18, 253–266. doi: 10.1017/S0031182000005217.CrossRefGoogle Scholar
Wenyon, C. M. and Sheather, L. (1925). Exhibition of specimens illustrating Isospora infections of dogs. [Proceedings of a Laboratory Meeting of the Society held at the Royal Army Medical College, Millibank, London, S.W.] Transactions of the Royal Society of Tropical Medicine and Hygiene 19, 10.Google Scholar