Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-28T04:57:16.807Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic characterization of Strongyloides spp. from captive, semi-captive and wild Bornean orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia

Published online by Cambridge University Press:  15 August 2011

E. M. LABES ,
N. WIJAYANTI ,
P. DEPLAZES  and
A. MATHIS
E. M. LABES
Affiliation:
University of Zurich, Institute of Parasitology, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
N. WIJAYANTI
Affiliation:
University Gadjah Mada, Centre for Biotechnology, 55281 Jogjakarta, Indonesia
P. DEPLAZES
Affiliation:
University of Zurich, Institute of Parasitology, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
A. MATHIS*
Affiliation:
University of Zurich, Institute of Parasitology, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
*
*Corresponding author: University of Zurich, Institute of Parasitology, Winterthurerstrasse 266a, 8057 Zurich, Switzerland. Tel: +41 (0)44 635 85 01. Fax: +41 (0)44 635 89 07. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Orangutans (Pongo spp.), Asia's only great apes, are threatened in their survival due to habitat loss, hunting and infections. Nematodes of the genus Strongyloides may represent a severe cause of death in wild and captive individuals. In order to better understand which Strongyloides species/subspecies infect orangutans under different conditions, larvae were isolated from fecal material collected in Indonesia from 9 captive, 2 semi-captive and 9 wild individuals, 18 captive groups of Bornean orangutans and from 1 human working with wild orangutans. Genotyping was done at the genomic rDNA locus (part of the 18S rRNA gene and internal transcribed spacer 1, ITS1) by sequencing amplicons. Thirty isolates, including the one from the human, could be identified as S. fuelleborni fuelleborni with 18S rRNA gene identities of 98·5–100%, with a corresponding published sequence. The ITS1 sequences could be determined for 17 of these isolates revealing a huge variability and 2 main clusters without obvious pattern with regard to attributes of the hosts. The ITS1 amplicons of 2 isolates were cloned and sequenced, revealing considerable variability indicative of mixed infections. One isolate from a captive individual was identified as S. stercoralis (18S rRNA) and showed 99% identity (ITS1) with S. stercoralis sequences from geographically distinct locations and host species. The findings are significant with regard to the zoonotic nature of these parasites and might contribute to the conservation of remaining orangutan populations.

Keywords

Strongyloides fuelleborniStrongyloides stercoralisgenomic rDNA locusBornean orangutanPongo pygmaeuszoonosis
Type
Research Article
Information
Parasitology , Volume 138 , Issue 11 , September 2011 , pp. 1417 - 1422
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ashford, R. W., Barnish, G. and Viney, M. E. (1992). Strongyloides fuelleborni kellyi: Infection and disease in Papua New Guinea. Parasitology Today 8, 314–318.CrossRefGoogle ScholarPubMed
Baldwin, B. G. (1992). Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the compositae. Molecular Phylogenetics and Evolution 1, 3–16.CrossRefGoogle ScholarPubMed
Collet, J. Y., Galdikas, B. M. F., Sugarjito, J. and Jojosudharmo, S. (1986). A coprological study of parasitism in orangutans (Pongo pygmaeus) in Indonesia. Journal of Medical Primatology 15, 121–129.CrossRefGoogle ScholarPubMed
Djojoasmoro, R. and Purnomo, A. (1998). Prevalensi nematoda usus pada orangutan di Taman Nasional Tanjung Puting Kalimantan Tengah. Journal of Primatology of Indonesia 2, 9–12.Google Scholar
Dorris, M., Viney, M. E. and Blaxter, M. L. (2002). Molecular phylogenetic analysis of the genus Strongyloides and related nematodes. International Journal for Parasitology 32, 1507–1517.CrossRefGoogle ScholarPubMed
Fisher, D., McCarry, F. and Currie, B. (1993). Strongyloidosis in the Northern Territory. Under-recognised and under-treated? Medical Journal of Australia 159, 88–90.CrossRefGoogle ScholarPubMed
Fisher, M. C. and Viney, M. E. (1998). The population genetic structure of the facultatively sexual parasitic nematode Strongyloides ratti in wild rats. Proceedings of the Royal Society of London, B 265, 703–709.CrossRefGoogle ScholarPubMed
Genta, R. (1989). Strongyloides stercoralis: loss of ability to disseminate after repeated passage in laboratory beagles. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 539–541.CrossRefGoogle ScholarPubMed
Gilles, H. M. and Cook, G. C. (1996). Soil-transmitted helminths (Geohelminths). In Manson's Tropical Disease (ed. Cook, G. C.), pp. 1369–1412. W. B. Saunders, London, UK.Google Scholar
Grove, D. I. (1989). Clinical manifestations. In Strongyloidiasis–a Major Roundworm Infection of Man (ed. Grove, D. I.). Taylor & Francis, London, UK.Google Scholar
Grove, D. I. and Northern, C. (1982). Infection and immunity in dogs infected with a human strain of Strongyloides stercoralis. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 833–838.CrossRefGoogle ScholarPubMed
Hasegawa, H., Hayashida, S., Ikeda, Y. and Sato, H. (2009). Hyper-variable regions in 18S rDNA of Strongyloides spp. as markers for species-specific diagnosis. Parasitology Research 104, 869–874. doi: 10.1007/s00436-008-1269-9CrossRefGoogle ScholarPubMed
Hira, P. R. and Patel, B. G. (1980). Human strongyloidiasis due to the primate species Strongyloides fülleborni. Tropical and Geographical Medicine 32, 23–29.Google Scholar
IUCN (2010). IUCN Red List of Threatened Species. IUCN, Gland, Switzerland. www.iucnredlist.orgGoogle Scholar
Labes, E. M., Hegglin, D., Grimm, F., Nurcahyo, W., Harrison, M. E., Bastian, M. L. and Deplazes, P. (2010). Intestinal parasites of endangered orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia. Parasitology 137, 123–135. doi: 10.1017/S0031182009991120CrossRefGoogle Scholar
Little, M. D. (1966). Comparative morphology of six species of Strongyloides (Nematoda) and redefinition of the genus. Journal of Parasitology 52, 69–84.CrossRefGoogle ScholarPubMed
Longo, M. C., Berninger, M. S. and Hartley, J. L. (1990). Use of uracil DNA glycosylase to control carry-over contamination in polymerase chain reactions. Gene 93, 125–128.CrossRefGoogle ScholarPubMed
Nolan, T. J., Genta, R. and Schad, G. A. (1998). Strongyloidosis. In Zoonoses (ed. Palmer, S. R., Soulsby, L. and Simpson, D. I. H.), pp. 747–758. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Ramachandran, S., Gam, A. A. and Neva, F. (1997). Molecular differences between several species of Strongyloides and comparison of selected isolates of S. stercoralis using a polymerase chain reaction-linked restriction fragment length polymorphism approach. American Journal of Tropical Medicine and Hygiene 56, 61–65.CrossRefGoogle ScholarPubMed
Rijksen, H. D. and Meijaard, E. (1999). A history of the orang-utan distribution. In Our Vanishing Relative: the Status of Wild Orang-utans at the Close of the Twentieth Century (ed. Rijksen, H. D. and Meijaard, E.), pp. 37–64. Kluwer Academic Publishers, Dordrecht, The Netherlands.CrossRefGoogle Scholar
Sato, H., Torii, H., Une, Y. and Ooi, H.-K. (2007). A new rhabditoid nematode species in Asian sciurids, distinct from Strongyloides robustus in North American Sciurids. Journal of Parasitology 93, 1476–1486.CrossRefGoogle ScholarPubMed
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Viney, M. E. (2006). The biology and genomics of Strongyloides. Medical Microbiology and Immunology 195, 49–54.CrossRefGoogle ScholarPubMed
Viney, M. E. and Lok, J. B. (2007). Strongyloides spp. In The C. elegans Research Community (ed. Viney, M. E. and Lok, J. B.), WormBook. doi: 10.1895/wormbook.1.141.1Google Scholar
Warren, K. S. (2001). Orangutan conservation – epidemiological aspects of health management and population genetics. Ph.D. thesis (pp. 73–83), Murdoch University, Australia.Google Scholar
Wells, S. K., Sargeant, E., Andrews, M. E. and Anderson, D. E. (1990). Gastrointestinal disorders. In Medical Management of the Orangutan (ed. Wells, S.), pp. 65–66. The Audobon Institute, New Orleans, Louisiana, USA.Google Scholar