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Insights into the epidemiology and genetic make-up of Oesophagostomum bifurcum from human and non-human primates using molecular tools

Published online by Cambridge University Press:  07 December 2005

R. B. GASSER ,
J. M. de GRUIJTER  and
A. M. POLDERMAN
R. B. GASSER
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia Biotechnology Research Institute, Macquarie University, Sydney, New South Wales 2109, Australia
J. M. de GRUIJTER
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia Department of Parasitology, Leiden University Medical Center, Leiden, PO Box 9605, 2300 RC Leiden, The Netherlands
A. M. POLDERMAN
Affiliation:
Department of Parasitology, Leiden University Medical Center, Leiden, PO Box 9605, 2300 RC Leiden, The Netherlands
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Abstract

The nodule worm Oesophagostomum bifurcum (Nematoda: Strongylida) is a parasite of major human health importance predominantly in northern Togo and Ghana. Currently, it is estimated that 0·25 million people are infected with this nematode, and at least 1 million people are at risk of infection. Infection with this parasite causes significant disease as a consequence of encysted larvae in the wall of the large intestine. In spite of the health problems caused by O. bifurcum, there have been significant gaps in the knowledge of the biology, transmission and population genetics of the parasite. This review provides an account of some recent insights into the epidemiology and genetics of the parasite from human and non-human primate hosts in specific regions of Africa using molecular tools. Recent research findings are discussed mainly in relation to non-human primates being reservoirs of infection, and the consequences for the prevention and control of oesophagostomiasis in humans are briefly discussed.

Keywords

Oesophagostomum bifurcumoesophagostomiasishumandiagnosismolecular toolsgeneticsepidemiologycontrol
Type
Review Article
Information
Parasitology , Volume 132 , Issue 4 , April 2006 , pp. 453 - 460
Copyright
2005 Cambridge University Press

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References

REFERENCES

Barger, L. A., Lewis, R. J. and Brown, G. F. ( 1984). Survival of infective larvae of nematode parasites of cattle during drought. Veterinary Parasitology 14, 143–152.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, 49–61.Google Scholar
Blouin, M. S. ( 2002). Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531.CrossRefGoogle Scholar
Chabaud, A. G. and Larivière, M. ( 1958). Sur les oesophagostomes parasites de l'homme. Bulletin de la Societé de Pathologie Exotique 51, 384–393.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, 229–237.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 10, 574–580.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, 183–188.CrossRefGoogle 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, 227–233.Google Scholar
Eberhard, M. L., Kovacs-Nace, E., Blotkamp, J., Verweij, J. J., Asigri, V. A. and Polderman, A. M. ( 2001). Experimental Oesophagostomum bifurcum in monkeys. Journal of Helminthology 75, 51–56.CrossRefGoogle Scholar
Elmes, B. G. T. and McAdam, J. W. J. ( 1954). Helminthic abscess, a surgical complication of oesophagostomes and hookworm. Annals of Tropical Medicine and Parasitology 48, 1–7.CrossRefGoogle Scholar
Gasser, R. B. ( 2001). Identification of parasitic nematodes and study of genetic variability using PCR approaches. (Chapter 4) In Parasitic Nematodes: Molecular Biology, Biochemistry and Immunology ( ed. Kennedy, M. W. and Harnett, W.), CABI Publishing, Oxon and New York, pp. 53–82.CrossRef
Gasser, R. B. ( 2005). Molecular tools – advances, opportunities and prospects. Veterinary Parasitology (in the Press).Google Scholar
Gasser, R. B., Woods, W. G., Blotkamp, J., Verweij, J., Storey, P. A. and Polderman, A. M. ( 1999). Screening for nucleotide variations in ribosomal DNA arrays of Oesophagostomum bifurcum by polymerase chain reaction-coupled single-strand conformation polymorphism. Electrophoresis 20, 1486–1491.3.0.CO;2-9>CrossRefGoogle Scholar
Gigase, P., Baeta, S., Kumar, V. and Brandt, J. ( 1987). Frequency of symptomatic human oesophagostomiasis (helminthoma) in northern Togo. In Helminth Zoonoses, ( ed. Geerts, S., Kumar, V. and Brandt, J.), pp. 233–236. Martinus Nijhoff, Dordrecht.
Glen, D. R. and Brooks, R. ( 1985). Phylogenetic relationships of some Strongylate nematodes of primates. Proceedings of the Helminthological Society of Washington 52, 227–236.Google Scholar
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. 101–137. Unwin Hyman, London.
Haaf, E. and van Soest, A. H. ( 1964). Oesophagostomiasis in man in North Ghana. Tropical and Geographical Medicine 16, 49–53.Google Scholar
Hotez, P. J., Bethony, J., Bottazzi, M. E., Brooker, S. and Buss, P. ( 2005). Hookworm: “The Great Infection of Mankind”. PLoS Medicine 2, e67.CrossRef
Hu, M., Chilton, N. B. and Gasser, R. B. ( 2004). The mitochondrial genomics of parasitic nematodes of socio-economic importance: recent progress, and implications for population genetics and systematics studies. Advances in Parasitology 56, 133–212.Google Scholar
Krepel, H. P. ( 1994). Oesophagostomum bifurcum infection in man: a study on the taxonomy, diagnosis, epidemiology and drug treatment of Oesophagostomum bifurcum in northern Togo and Ghana. Ph.D. thesis. Leiden University, The Netherlands.
Krepel, H. P., Baeta, S. and Polderman, A. M. ( 1992). Human Oesophagostomum infection in northern Togo and Ghana: epidemiological aspects. Annals of Tropical Medicine and Parasitology 86, 289–300.CrossRefGoogle Scholar
Krepel, H. P., Haring, T., Baeta, S. and Polderman, A. M. ( 1993). Treatment of mixed Oesophagostomum and hookworm infection: effect of albendazole, pyrantel pamoate, levamisole and thiabendazole. Transactions of the Royal Society of Tropical Medicine and Hygiene 87, 87–89.CrossRefGoogle Scholar
Krepel, H. P. and Polderman, A. M. ( 1992). Egg production of Oesophagostomum bifurcum, a locally common parasite of humans in Togo. American Journal of Tropical Medicine and Hygiene 46, 469–472.CrossRefGoogle Scholar
Leiper, R. T. ( 1911). The occurence of Oesophagostomum apiostomum as an intestinal parasite of man in Nigeria. Journal of Tropical Medicine and Hygiene 14, 116–118.Google Scholar
van Lieshout, L., de Gruijter, J. M., Adu-Nsiah, M., Haizel, M., Verweij, J. J., Brienen, E. A. T., Gasser, R. B. and Polderman, A. M. ( 2005). Observations on Oesophagostomum bifurcum in non-human primates, a potential reservoir for human infection in Ghana? Tropical Medicine and International Health. (in the Press.)Google Scholar
Polderman, A. M., Anemana, S. D. and Asigri, V. ( 1999). Human oesophagostomiasis: a regional public health problem in Africa. Parasitology Today 15, 129–130.CrossRefGoogle Scholar
Polderman, A. M. and Blotkamp, J. ( 1995). Oesophagostomum infections in humans. Parasitology Today 11, 451–460.CrossRefGoogle Scholar
Polderman, A. M., Krepel, H. P., Baeta, S., Blotkamp, J. and Gigase, P. ( 1991). Oesophagostomiasis, a common infection of man in northern Togo and Ghana. American Journal of Tropical Medicine and Hygiene 44, 336–344.CrossRefGoogle Scholar
Pit, D. S., Rijcken, F. E., Raspoort, E. C., Baeta, S. M. and Polderman, A. M. ( 1999 a). Geographic distribution and epidemiology of Oesophagostomum bifurcum and hookworm infections in humans in Togo. American Journal of Tropical Medicine and Hygiene 61, 951–955.Google Scholar
Pit, D. S., de Graaf, W., Snoek, H., de Vlas, S. J., Baeta, S. M. and Polderman, A. M. ( 1999 b). Diagnosis of Oesophagostomum bifurcum and hookworm infection in humans: day-to-day and within-specimen variation of larval counts. Parasitology 118, 283–288.Google Scholar
Pit, D. S., Blotkamp, J., Polderman, A. M., Baeta, S. and Eberhard, M. L. ( 2000). The capacity of the third-stage larvae of Oesophagostomum bifurcum to survive adverse conditions. Annals of Tropical Medicine and Parasitology 94, 165–171.CrossRefGoogle Scholar
Romstad, A., Gasser, R. B., Monti, J. R., Polderman, A. M., Nansen, P., Pit, D. S. and Chilton, N. B. ( 1997 a). Differentiation of Oesophagostomum bifurcum from Necator americanus by PCR using genetic markers in spacer ribosomal DNA. Molecular and Cellular Probes 11, 169–176.Google Scholar
Romstad, A., Gasser, R. B., Nansen, P., Polderman, A. M., Monti, J. R. and Chilton, N. B. ( 1997 b). Characterization of Oesophagostomum bifurcum and Necator americanus by PCR-RFLP of rDNA. Journal of Parasitology 83, 963–966.Google Scholar
Rose, J. H. and Small, A. J. ( 1980). Observations on the development and survival of the free-living stages of Oesophagostomum dentatum both in their natural environments out-of-doors and under controlled conditions in the laboratory. Parasitology 81, 507–517.CrossRefGoogle Scholar
Schindler, A. R., de Gruijter, J. M., Polderman, A. M. and Gasser, R. B. ( 2005). Definition of genetic markers in nuclear ribosomal DNA for a neglected parasite of primates, Ternidens deminutus (Nematoda: Strongylida) – diagnostic and epidemiological implications. Parasitology 131, 539–546.CrossRefGoogle Scholar
Skrjabin, K. I., Shikhobalova, N. P., Schulz, R. S., Popova, T. I., Boev, S. N. and Delyamure, S. L. ( 1991). Strongylata. In Keys to Parasitic Nematodes Vol. 3 ( ed. Skrjabin, K. I.), pp. 230–247. [English Translation of Opredelitel' Paraziticheskikh Nematod. Izdatel'stvo Akademii Nauk SSSR, Moscow]. Amerind Publishing Co. Pvt. Ltd, New Dehli.
Spindler, L. A. ( 1936). Effects of various physical factors on survival of eggs and infective larvae of the swine nodular worm Oesophagostomum dentatum. Parasitology 22, 259.Google Scholar
Stewart, T. B. and Gasbarre, L. C. ( 1989). The veterinary importance of nodular worms (Oesophagostomum spp.). Parasitology Today 5, 209–213.CrossRefGoogle Scholar
Storey, P. A., Bugri, S., Magnussen, P. and Polderman, A. M. ( 2001 b). The effect of albendazole on Oesophagostomum bifurcum infection and pathology in children from rural northern Ghana. Annals of Tropical Medicine and Parasitology 95, 87–95.Google Scholar
Storey, P. A., Faile, G., Hewitt, E., Yelifari, L., Polderman, A. M. and Magnussen, P. ( 2000). Clinical epidemiology and classification of human oesophagostomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 177–182.CrossRefGoogle Scholar
Storey, P. A., Steenhard, N. R., van Lieshout, L., Anemana, S., Magnussen, P. and Polderman, A. M. ( 2001 a). Natural progression of Oesophagostomum bifurcum pathology and infection in a rural community of northern Ghana. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 295–299.Google Scholar
van Lieshout, L., de Gruijter, J. M., Adu-Nsiah, M., Haizel, M., Verweij, J. J., Brienen, E. A. T., Gasser, R. B. and Polderman, A. M. ( 2005). Observations on Oesophagostomum bifurcum in non-human primates, a potential reservoir for human infection in Ghana? Tropical Medicine and International Health (in the Press.)Google Scholar
Verweij, J. J., Pit, D. 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, 726–731.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, 137–142.CrossRefGoogle Scholar
Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J. and Kuiper, M. ( 1995). AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23, 4407–4414.CrossRefGoogle Scholar
Welsh, J. and McClelland, M. ( 1990). Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Research 18, 7213–7218.CrossRefGoogle Scholar
Williams, J. G., Kubelik, A. R., Livak, K. J., Rafalski, J. A. and Tingey, S. V. ( 1990). DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Research 18, 6531–6535.CrossRefGoogle Scholar
Yelifari, L., Bloch, P., Magnussen, P., van Lieshout, L., Dery, G., Anemana, S., Agongo, E. and Polderman, A. M. ( 2005). Distribution of human Oesophagostomum bifurcum, hookworm and Strongyloides stercoralis infections in northern Ghana. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 32–38.CrossRefGoogle Scholar
Ziem, J. B., Kettenis, I. M., Bayita, A., Brienen, E. A., Dittoh, S., Horton, J., Olsen, A., Magnussen, P. and Polderman, A. M. ( 2004). The short-term impact of albendazole treatment on Oesophagostomum bifurcum and hookworm infections in northern Ghana. Annals of Tropical Medicine and Parasitology 98, 385–390.CrossRefGoogle Scholar
Ziem, J. B., Spannbrucker, N., Magnussen, P., Olsen, A., Amon-Kotey, D. N., Frenzel, K., Nang-Beifubah, A., Westendorp, R. G. and Polderman, A. M. ( 2005). Oesophagostomum bifurcum-induced nodular pathology in a highly endemic area of Northern Ghana. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 417–422.CrossRefGoogle Scholar