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Definition of genetic markers in nuclear ribosomal DNA for a neglected parasite of primates, Ternidens deminutus (Nematoda: Strongylida) – diagnostic and epidemiological implications

Published online by Cambridge University Press:  23 May 2005

A. R. SCHINDLER
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
J. M. DE GRUIJTER
Affiliation:
Department of Parasitology, Leiden University Medical Center, University of Leiden, PO Box 9605, 2300 RC Leiden, The Netherlands
A. M. POLDERMAN
Affiliation:
Department of Parasitology, Leiden University Medical Center, University of Leiden, PO Box 9605, 2300 RC Leiden, The Netherlands
R. B. GASSER
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia

Abstract

Ternidens deminutus (Strongylida) is a parasitic nematode infecting non-human and human primates in parts of Africa, Asia and the Pacific islands. The present study genetically characterized T. deminutus and defined genetic markers in nuclear ribosomal DNA (rDNA) as a basis for developing molecular-diagnostic tools. The sequences of the second internal transcribed spacer (ITS-2) of rDNA were determined for adult specimens of T. deminutus (Nematoda: Strongylida: Oesophagostominae) from the Olive baboon and the Mona monkey.Nucleotide sequence data used in this paper are available in the EMBL, GenBank and DDJB databases under the Accession nos. AJ888729, AJ888730, AF136576, Y10789, Y10790, Y11733, Y11735, Y11736, AJ001594, AJ001599, AJ006149 and AJ006150. The former 2 sequences represent original data reported in this paper. The length and G+C content of the ITS-2 sequences was 216 bp and ~43%, respectively. While there was no sequence variation among individual T. deminutus specimens from the baboon, 6 (2·8%) nucleotide differences were detected in the ITS-2 between the parasite from baboon and that of the Mona monkey, which is similar to the difference (3·2%) between 2 other species of Oesophagostominae (Oesophagostomum bifurcum and O. stephanostomum) from non-human primates, suggesting significant population variation or the existence of cryptic (i.e. hidden) species within T. deminutus. Pairwise comparisons of the ITS-2 sequences of the 2 operational taxonomic units of T. deminutus with previously published ITS-2 sequences for selected members of the subfamilies Oesophagostominae and Chabertiinae indicated that species from primates (including those representing the subgenera Conoweberia and Ihleia) are closely related, in accordance with previous morphological studies. The sequence differences (27–48·3%) in the ITS-2 between the 2 taxonomic units of T. deminutus and hookworms (superfamily Ancylostomatoidea) enabled their identification and delineation by polymerase chain reaction (PCR)-based mutation scanning. The genetic markers in the ITS-2 provide a foundation for improved, PCR-based diagnosis of T. deminutus infections and for investigating the life-cycle, transmission patterns and ecology of this parasite.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Amberson, J. M. and Schwarz, E. ( 1952). Ternidens deminutus Railliet and Henry, a nematode parasite of man and primates. Annals of Tropical Medicine and Parasitology 46, 227237.CrossRefGoogle Scholar
Blotkamp, J., Krepel, K. P., Kumar, V., Baeta, S., van't Noorende, J. M. and Polderman, A. M. ( 1993). Observations on the morphology of adults and larval stages of Oesophagostomum sp. isolated from man in northern Togo and Ghana. Journal of Helminthology 67, 4961.Google Scholar
Chilton, N. B. and Gasser, R. B. ( 1999). Sequence differences in the internal transcribed spacers of DNA among four species of hookworm (Ancylostomatoidea: Ancylostoma). International Journal for Parasitology 29, 19711977.CrossRefGoogle Scholar
Chilton, N. B., Gasser, R. B. and Beveridge, I. ( 1995). Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). International Journal for Parasitology 25, 647651.CrossRefGoogle Scholar
Chilton, N. B., Gasser, R. B. and Beveridge, I. ( 1997). Phylogenetic relationships of Australian strongyloid nematodes inferred from ribosomal DNA sequence data. International Journal for Parasitology 27, 14811494.CrossRefGoogle Scholar
Chilton, N. B., Hoste, H., Newton, L. A., Beveridge, I. and Gasser, R. B. ( 1998). Common secondary structures for the second internal transcribed spacer pre-rRNA of two subfamilies of trichostrongylid nematodes. International Journal for Parasitology 28, 17651773.CrossRefGoogle Scholar
Chilton, N. B., Newton, L. A., Beveridge, I. and Gasser, R. B. ( 2001). Evolutionary relationships of trichostrongyloid nematodes (Strongylida) inferred from ribosomal DNA sequence data. Molecular Phylogenetics and Evolution 19, 367386.CrossRefGoogle Scholar
Cook, G. C. ( 1986). The clinical significance of gastrointestinal helminths – a review. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 675685.CrossRefGoogle Scholar
Gasser, R. B. ( 1999). PCR-based technology in veterinary parasitology. Veterinary Parasitology 84, 229258.CrossRefGoogle Scholar
Gasser, R. B. ( 2001). Identification of parasitic nematodes and study of genetic variability using PCR approaches. In Parasitic Nematodes: Molecular Biology, Biochemistry and Immunology (ed. Kennedy, M. W. and Harnett, W.), pp. 5382. CABI Publishing, CAB International, Wallingford, UK.CrossRef
Gasser, R. B., Chilton, N.B., Hoste, H. and Beveridge, I. ( 1993). Rapid sequencing of rDNA from single worms and eggs of parasitic helminths. Nucleic Acids Research 21, 25252526.CrossRefGoogle Scholar
Gasser, R. B., Hu, M., Abs EL-Osta, Y. G., Zarlenga, D. S. and Pozio, E. ( 2004 b). Non-isotopic single-strand conformation polymorphism analysis of sequence variability in ribosomal DNA expansion segments within the genus Trichinella (Nematoda: Adenophorea). Electrophoresis 25, 33573364.Google Scholar
Gasser, R. B., Hung, G.-C., Chilton, N. B. and Beveridge, I. ( 2004 a). Advances in developing molecular-diagnostic tools for strongyloid nematodes of equids: fundamental and applied implications. Molecular and Cellular Probes 18, 316.Google Scholar
Gasser, R. B., Woods, W. G., Blotkamp, J., Verweij, J., Storey, P. A. and Polderman, A. M. ( 1999 a). Screening for nucleotide variations in ribosomal DNA arrays of Oesophagostomum bifurcum by PCR-coupled single-strand conformation polymorphism. Electrophoresis 20, 14861491.Google Scholar
Gasser, R. B., Woods, W. G., Huffman, M. A., Blotkamp, J. and Polderman, A. M. ( 1999 b). Molecular separation of Oesophagostomum stephanostomum and Oesophagostomum bifurcum (Nematoda: Strongyloidea) from non-human primates. International Journal for Parasitology 29, 10871091.Google Scholar
Goldsmid, J. M. ( 1971 a). Ternidens deminutus: a parasitological enigma in Rhodesia. Research Lecture Series No. 4. Faculty of Medicine, University of Rhodesia.
Goldsmid, J. M. ( 1971 b). Studies on the life cycle and biology of Ternidens deminutus (Railliet and Henry, 1909) (Nematoda: Strongylidae). Journal of Helminthology 45, 341352.Google Scholar
Goldsmid, J. M. ( 1972). Ternidens deminutus (Railliet and Henry, 1909) and hookworm in Rhodesia and a review of the treatment of human infections with Ternidens deminutus. Central African Journal of Medicine 18 (Suppl.), 114.Google Scholar
Goldsmid, J. M. ( 1974). The intestinal helminthozoonoses of primates in Rhodesia. Annales de la Société Belge de Medecine Tropicale 54, 87101.Google Scholar
Goldsmid, J. M. ( 1982). Ternidens infection. In Handbook Series in Zoonoses (ed. Steele, H.). Section C: Parasitic Zoonoses, Vol. 2, pp. 269288. CRC Press, Boca Raton, Florida.
Goldsmid, J. M. ( 1991). The African hookworm problem: an overview. In Parasitic Helminths and Zoonoses in Africa (ed. MacPherson, C. N. L. and Craig, P. S.), pp. 101137. Unwin Hyman, London.
Goldsmid, J. M. and Lyons, N. F. ( 1973). Studies on Ternidens deminutus Railliet and Henry, 1909 (Nematoda). I. External morphology. Journal of Helminthology 47, 119126.Google Scholar
de Gruijter, J. M., Gasser, R. B., Polderman, A. M., Asigri, V. and Dijkshoorn, L. ( 2005 a). High resolution DNA fingerprinting by AFLP to study the genetic variation among Oesophagostomum bifurcum (Nematoda) from human and non-human primates in Ghana. Parasitology 130, 229237.Google Scholar
de Gruijter, J. M., van Lieshout, L., Gasser, R. B., Verweij, J. J., Brienen, E. A. T., Ziem, J. B., Yelifari, L. and Polderman, A. M. ( 2005 b). PCR-based differential diagnosis of Ancylostoma duodenale and Necator americanus in humans from northern Ghana. Tropical Medicine and International Health. (in the Press).Google Scholar
de Gruijter, J. M., Polderman, A. M., Zhu, X. Q. and Gasser, R. B. ( 2002). Screening for haplotypic variability within Oesophagostomum bifurcum (Nematoda) employing a single-strand conformation polymorphism approach Molecular and Cellular Probes 16, 185190.Google Scholar
de Gruijter, J. M., Ziem, J., Verweij, J. J., Polderman, A. M. and Gasser, R. B. ( 2004). Genetic substructuring within Oesophagostomum bifurcum (Nematoda) from human and non-human primates from Ghana based on random amplification of polymorphic DNA analysis. American Journal of Tropical Medicine and Hygiene 71, 227233.Google Scholar
Hotez, P. J., Brooker, S., Bethony, J. M., Bottazzi, M. E., Loukas, A. and Xiao, S. ( 2004). Hookworm infection. New England Journal of Medicine 351, 799807.CrossRefGoogle Scholar
Hung, G.-C., Chilton, N. B., Beveridge, I. and Gasser, R. B. ( 2000). A molecular systematic framework for equine strongyles based on DNA sequence data. International Journal for Parasitology 30, 95103.CrossRefGoogle Scholar
Kato, K. and Miura, M. ( 1954). On the comparison of some stool examination methods. Japanese Journal of Parasitology 3, 35. [In Japanese.]Google Scholar
Kilala, C. P. ( 1971). Ternidens deminutus infecting man in southern Tanzania. East African Medical Journal 48, 636645.Google Scholar
Martin, L. K. and Beaver, P. C. ( 1968). Evaluation of Kato thick-smear technique for quantitative diagnosis of helminth infections. American Journal of Tropical Medicine and Hygiene 17, 382391.CrossRefGoogle Scholar
Newton, L. A., Chilton, N. B., Beveridge, I. and Gasser, R. B. ( 1998). Systematic relationships of some members of the genera Oesophagostomum and Chabertia (Nematoda: Chabertiidae) based on ribosomal DNA sequence data. International Journal for Parasitology 28, 17811789.CrossRefGoogle Scholar
Polderman, A. M. and Blotkamp, J. ( 1995). Oesophagostomum infections in humans. Parasitology Today 11, 451456.CrossRefGoogle Scholar
Ridley, D. S. and Hawgood, B. C. ( 1956). The value of formol-ether concentration of faecal cysts and ova. Journal of Clinical Pathology 9, 7476.CrossRefGoogle Scholar
Romstad, A., Gasser, R. B., Monti, J. R., Polderman, A. M., Nansen, P., Pit, D. S. S. and Chilton, N. B. ( 1997). Differentiation of Oesophagostomum bifurcum from Necator americanus by PCR using genetic markers in spacer ribosomal DNA. Molecular and Cellular Probes 11, 169176.CrossRefGoogle Scholar
Romstad, A., Gasser, R. B., Nansen, P., Polderman, A. M. and Chilton, N. B. ( 1998). Necator americanus (Nematoda: Ancylostomatidae) from Africa and Malaysia have different ITS-2 rDNA sequences. International Journal for Parasitology 28, 611615.CrossRefGoogle Scholar
Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B. and Erlich, H. A. ( 1988). Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239, 487491.CrossRefGoogle Scholar
Sandground, J. H. ( 1929). Ternidens deminutus (Railliet and Henry) as a parasite of man in Southern Rhodesia; together with observations and experimental infection studies on an unidentified parasite of man from this region. Annals of Tropical Medicine and Parasitology 23, 2332.CrossRefGoogle Scholar
Sandground, J. H. ( 1931). Studies on the life-history of Ternidens deminutus, a nematode parasite of man, with observations on its incidence in certain regions of Southern Africa. Annals of Tropical Medicine and Parasitology 25, 147184.CrossRefGoogle Scholar
Skrjabin, K. I., Shikhobalova, N. P., Schulz, R. S., Popova, T. I., Boev, S. N. and Delyamure, S. L. ( 1952). Strongylata. In Keys to Parasitic Nematodes Vol. 3 (ed. Skrjabin, K. I.), E. J. Brill, New York [English Translation; Israel Program for Scientific Translation, 1961, Jerusalem].
Thompson, J. D., Higgins, D. G. and Gibson, T. J. ( 1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.CrossRefGoogle Scholar
Van den Berghe, I. ( 1934). L'existence de Ternidens deminutus au Katanga. Annales de la Société Belge de Medecine Tropicale 41, 189.Google Scholar
Verweij, J. J., Pit, D. S. S., van Lieshout, L., Baeta, S. M., Dery, G. D., Gasser, R. B. and Polderman, A. M. ( 2001). Determining the prevalence of Oesophagostomum bifurcum and Necator americanus infections using specific PCR amplification of DNA from faecal samples. Tropical Medicine and International Health 6, 726731.CrossRefGoogle Scholar
Verweij, J. J., Polderman, A. M., Wimmenhove, M. C. and Gasser, R. B. ( 2000). PCR assay for the specific amplification of Oesophagostomum bifurcum DNA from human faeces. International Journal for Parasitology 30, 137142.CrossRefGoogle Scholar