Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T22:38:16.177Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphology and surface topography of the schistosome Bivitellobilharzia nairi from the Asian elephant (Elephas maximus maximus) in Sri Lanka

Published online by Cambridge University Press:  19 September 2012

R.P.V.J. Rajapakse ,
M. Iwagami ,
S. Wickramasinghe ,
S.M. Walker  and
T. Agatsuma
R.P.V.J. Rajapakse*
Affiliation:
Department of Veterinary Pathobiology, Faculty of Veterinary Medicine and Animal Science, University of Peradeniya, Peradeniya, Sri Lanka
M. Iwagami
Affiliation:
Department of Environmental Health Sciences, Kochi Medical School, Kochi University, Oko, Nankoku City, Kochi783-8505, Japan
S. Wickramasinghe
Affiliation:
Department of Veterinary Pathobiology, Faculty of Veterinary Medicine and Animal Science, University of Peradeniya, Peradeniya, Sri Lanka
S.M. Walker
Affiliation:
Medical Biology Centre, School of Biological Sciences, Queen's University Belfast, 97 Lisburn Road, BelfastBT9 7BL, UK
T. Agatsuma
Affiliation:
Department of Environmental Health Sciences, Kochi Medical School, Kochi University, Oko, Nankoku City, Kochi783-8505, Japan
*
* E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Bivitellobilharzia nairi was first recorded from an Indian elephant (Elephas maximus) in Berlin. Infections with this parasite have become increasingly important in E. maximus maximus populations in Sri Lanka. The present work is the first morphological description of this schistosome from Sri Lanka. A number of adult worms were recovered from a dead Asian elephant near the elephant orphanage, Pinnawala, in Sri Lanka. The observed clinical features of the infected elephant included emaciation, subventral oedema and anaemia. Post-mortem results indicated that the liver was enlarged and adult schistosomes were found in the blood vessels of the liver parenchyma. The total number of worms recovered from a portion of the liver was 129,870, which is an average of 22 worms per 100 g of liver. The present study uses both light microscopic and scanning electron microscope (SEM) techniques for the morphological and topographical characterization of this parasite and to permit comparison with other species of schistosomes. Morphologically, these worms correspond very well to the description of B. nairi by Dutt & Srivastava (1955). Moreover, it is clear that B. nairi is a distinctive species easily differentiated from other schistosomes. The SEM study of the tegument of male worms shows that the surface of B. nairi is smoother than in other schistosomes.

Type
Research Papers
Information
Journal of Helminthology , Volume 87 , Issue 3 , September 2013 , pp. 348 - 355
Copyright
Copyright © Cambridge University Press 2012 

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

Agatsuma, T., Iwagami, M., Liu, C.X., Rajapakse, R.P.V.J., Mondal, M.M.H., Kitikoon, V., Ambu, S., Agatsuma, Y., Blair, D. & Higuchi, T. (2002) Affinity between Asian non-human Schistosoma species, the S. indicum group and the African human schistosomes. Journal of Helminthology 76, 7–19.CrossRefGoogle Scholar
Agatsuma, T., Rajapakse, R.P.V.J., Kuruwita, V.Y., Iwagami, M. & Rajapakse, R.C. (2004) Molecular taxonomic position of the elephant schistosome, Bivitellobilharzia nairi, newly discovered in Sri Lanka. International Journal for Parasitology 53, 69–75.CrossRefGoogle ScholarPubMed
Basch, P.F. (1991) Schistosomes: Development, reproduction and host relations. 408 pp. Oxford, Oxford University Press.Google Scholar
Brant, S.V., Morgan, J.A.T., Mkoji, G.M., Snyder, S.D., Rajapakse, R.P.V.J. & Loker, E.S. (2006) An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of key reference data including DNA sequence from single life cycle stages. Journal of Parasitology 92, 77–88.CrossRefGoogle ScholarPubMed
Dutt, S.C. & Srivastava, H.D. (1952) On the morphology and life history of a new mammalian blood-fluke – Ornithobilharzia dattai N.SP (Preliminary report). Parasitology 42, 144–149.CrossRefGoogle ScholarPubMed
Dutt, S.C. & Srivastava, H.D. (1955) A revision of genus Ornithobilharzia Odhner, 1912. (Trematoda: Schistosomatidae). Proceedings of the Indian Science Congress 42, 283.Google Scholar
Dutt, S.C. & Srivastava, H.D. (1961) A revision of the genus Ornithobilharzia Odhner, 1912, with the creation of two genera: Orientobilharzia Dutt and Srivastava (1955) and Sinobilharzia Dutt, S.C. & Srivastava, H.D. (1955) (Trematoda: Schistosomatidae). Indian Journal of Helminthology 13, 61–73.Google Scholar
Farley, J. (1971) A review of the family Schistosomatidae: excluding the genus Schistosoma from mammals. Journal of Helminthology XLV, 289–320.CrossRefGoogle ScholarPubMed
Fried, B. & Manger, P.M. Jr (1992) Use of an aceto-carmine procedure to examine the excysted metacercariae of Echinostoma caproni and E. trivolvis. Journal of Helminthology 66, 238–240.CrossRefGoogle ScholarPubMed
Hicks, R.M. & Newman, J. (1977) The surface structure of the tegument of Schistosoma haematobium. Cell Biology International Reports 1, 157–167.CrossRefGoogle ScholarPubMed
Kruatrachue, M., Bhaibulaya, M. & Harinasuta, C. (1965) Orientobilharzia harinasutai sp.nov. a mammalian blood-fluke, its morphology and life-cycle. Annals of Tropical Medicine and Parasitology 59, 181–188.CrossRefGoogle ScholarPubMed
Kruatrachue, M., Riengrojpitak, S., Sahaphong, S. & Upatham, E.S. (1982) Scanning electron microscopy of adult Schistosoma incognitum. Southeast Asian Journal of Tropical Medicine and Public Health 13, 163–173.Google ScholarPubMed
Kruatrachue, M., Riengrojpitak, S., Upatham, E.S. & Sahaphong, S. (1983a) Scanning electron microscopy of the tegumental surface of adult Schistosoma spindale. Southeast Asian Journal of Tropical Medicine and Public Health 14, 281–289.Google ScholarPubMed
Kruatrachue, M., Upatham, E.S., Sahaphong, S., Tongthong, T. & Khunborivan, V. (1983b) Scanning electron microscopic study of the tegumental surface of adult Schistosoma sinensium. Southeast Asian Journal of Tropical Medicine and Public Health 14, 427–438.Google ScholarPubMed
Kruatrachue, M., Upatham, E.S., Sahaphong, S., Tongthong, T. & Khunborivan, V. (1987) Scanning electron microscopic study of the tegumental surface of the hybrid schistosome between Schistosoma mekongi and S. japonicum-like (Malaysian). Southeast Asian Journal of Tropical Medicine and Public Health 18, 453–466.Google ScholarPubMed
Kuntz, R.E., Tulloch, G.S., Davidson, D.L. & Huang, T.C. (1976) Scanning electron microscopy of the integumental surfaces of Schistosoma haematobium. Journal of Parasitology 62, 63–69.CrossRefGoogle ScholarPubMed
Kuntz, R.E., Tulloch, G.S., Huang, T.C. & Davidson, D.L. (1977) Scanning electron microscopy of integumental surfaces of Schistosoma intercalatum. Journal of Parasitology 63, 401–406.CrossRefGoogle ScholarPubMed
Kuntz, R.E., Davidson, D.L., Huang, T.C. & Tulloch, G.S. (1979) Scanning electron microscopy of the integumental surfaces of Schistosoma bovis. Journal of Helminthology 53, 131–132.CrossRefGoogle ScholarPubMed
Lockyer, A.E., Olson, P.D., Ostergaard, P., Rollinson, D., Johnston, D.A., Attwood, S.W., Southgate, V.R., Horak, P., Snyder, S.D., Le, T.H., Agatsuma, T., McManus, D.P., Carmichael, A.C., Naem, S. & Littlewood, D.T.J. (2003) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203–224.CrossRefGoogle ScholarPubMed
McKinstry, B., Fairweather, I., Brennan, G.P. & Forbes, A.B. (2003) Fasciola hepatica: tegumental surface alterations following treatment in vivo and in vitro with nitroxynil (Trodax). Parasitology Research 91, 251–263.CrossRefGoogle ScholarPubMed
Miller, F.H. Jr, Tulloch, G.S. & Kuntz, R.E. (1972) Scanning electron microscopy of integumental surface of Schistosoma mansoni. Journal of Parasitology 58, 693–698.CrossRefGoogle ScholarPubMed
Morris, G.P. & Threadgold, T. (1968) Ultrastructure of the tegument of adult Schistosoma mansoni. Journal of Parasitology 54, 15–17.CrossRefGoogle ScholarPubMed
Mudaliar, S.V. & Ramanujachary, G. (1945) Schistosoma nairi n.sp. from an elephant. The Indian Veterinary Journal 12, 1–5.Google Scholar
Platt, T.R. & Brooks, D.R. (1997) Evolution of the schistosomes (Digenea: Schistosomatoidea): the origin of dioecy and colonization of the venous system. Journal of Parasitology 83, 1035–1045.CrossRefGoogle ScholarPubMed
Robert, E.K., George, S.T., David, L.D. & Too-cheng, H. (1976) Scanning electron microscopy of integumental surfaces of Schistosoma haematobium. Journal of Parasitology 62, 63–69.Google Scholar
Robert, E.K., George, S.T., Too-cheng, H. & David, L.D. (1977) Scanning electron microscopy of integumental surfaces of Schistosoma intercalatum. Journal of Parasitology 63, 401–406.Google Scholar
Rollinson, D. & Southgate, V.R. (1987) The genus Schistosoma: A taxonomic appraisal. pp. 1–49in Rollinson, D. & Simpson, A.J.G. (Eds) The biology of schistosomes: From genus to latrines. London, Academic Press.Google Scholar
Senft, A.W., Philpott, D.E. & Pelofsky, A.H. (1961) Electron microscope observations of the integument, flame cells, and gut of Schistosoma mansoni. Journal of Parasitology 47, 217–229.CrossRefGoogle ScholarPubMed
Smith, J.H., Reynolds, E.S. & Von Lichtenberg, F. (1969) The integument of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 18, 28–49.CrossRefGoogle ScholarPubMed
Snyder, S.D. & Loker, E.S. (2000) Evolutionary relationships among the Schistosomatidae (Platyhelminthes: Digenea) and an Asian origin for Schistosoma. Journal of Parasitology 86, 283–288.CrossRefGoogle Scholar
Sobhon, P., Upatham, E.S., Koonchornboon, T., Saitongdee, P., Khunborivan, V., Yuan, H.C., Vongpayabal, P., Ow-Yang, C.K. & Greer, G.J. (1983) Microtopography of the surface of adult Schistosoma japonicum-like (Malaysian) as observed by scanning electron microscopy. Southeast Asian Journal of Tropical Medicine and Public Health 14, 439–450.Google ScholarPubMed
Sobhon, P., Upatham, E.S. & McLaren, D.J. (1984) Topography and ultrastructure of the tegument of adult Schistosoma mekongi. Parasitology 89, 511–521.CrossRefGoogle ScholarPubMed
Southgate, V.R., Rollinson, D. & Vercruysse, J. (1986) Scanning electron microscopy of the tegument of adult Schistosoma curassoni, and comparison with male S. bovis and S. haematobium from Senegal. Parasitology 93, 433–442.CrossRefGoogle Scholar
Stunkard, H.W. & Hinchcliffe, M.C. (1952) The morphological and life history of Microbilharzia variglandis (Miller and Northup, 1926) Stunkard and Hinchcliffe, 1951, avian blood-flukes whose larvae cause ‘swimmers itch’ of ocean beaches. Journal of Parasitology 38, 248–265.CrossRefGoogle Scholar
Thurston, P.J. (1963) Schistosomes from Hippopotamus amphibious L. I. The morphology of Schistosoma hippopotami sp.nov. Parasitology 53, 49–54.CrossRefGoogle Scholar
Tulloch, G.S., Kuntz, R.E., Davidson, D.L. & Huang, T.C. (1977) Scanning electron microscopy of the integument of Schistosoma mattheei Veglia & Le Roux, 1929. Transactions of the American Microscopical Society 96, 41–47.CrossRefGoogle Scholar
Vogel, H. von & Minning, W. (1940) Bilharziose bei elephanten. Archiv fur Schiffs Tropen-Hygiene 44, 562–574.Google Scholar
Vongpayabal, P., Sobhon, P., Upatham, E.S., Wanichanon, C., Mitranond, V., Tanphaichitr, N. & Tumbel, V.E. (1982) Scanning electron microscopic study of the tegumental surface of adult Schistosoma mekongi. Parasitology 85, 325–332.CrossRefGoogle ScholarPubMed
Yamaguti, S. (1958) Systema helminthum, Vol. 1. The digenetic trematodes of vertebrates. 575 pp. New York, Interscience Publication Inc.Google Scholar