Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-13T01:48:58.278Z Has data issue: false hasContentIssue false

Schistosomes of small mammals from the Lake Victoria Basin, Kenya: new species, familiar species, and implications for schistosomiasis control

Published online by Cambridge University Press:  12 April 2010

B. HANELT*
Affiliation:
Department of Biology, University of New Mexico, MSC03 2020, Albuquerque, New Mexico, 87131-0001, USA
I. N. MWANGI
Affiliation:
Center for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, P.O. Box 54840-00200, City Square, Nairobi, Kenya
J. M. KINUTHIA
Affiliation:
Center for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, P.O. Box 54840-00200, City Square, Nairobi, Kenya
G. M. MAINA
Affiliation:
Center for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, P.O. Box 54840-00200, City Square, Nairobi, Kenya
L. E. AGOLA
Affiliation:
Center for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, P.O. Box 54840-00200, City Square, Nairobi, Kenya
M. W. MUTUKU
Affiliation:
Center for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, P.O. Box 54840-00200, City Square, Nairobi, Kenya
M. L. STEINAUER
Affiliation:
Department of Biology, University of New Mexico, MSC03 2020, Albuquerque, New Mexico, 87131-0001, USA
B. R. AGWANDA
Affiliation:
National Museum of Kenya, Zoology Department, Mammal Section, Museum Hill Road, P.O. Box 40658, Westlands, Nairobi, Kenya
L. KIGO
Affiliation:
National Museum of Kenya, Zoology Department, Mammal Section, Museum Hill Road, P.O. Box 40658, Westlands, Nairobi, Kenya
B. N. MUNGAI
Affiliation:
Center for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, P.O. Box 54840-00200, City Square, Nairobi, Kenya
E. S. LOKER
Affiliation:
Department of Biology, University of New Mexico, MSC03 2020, Albuquerque, New Mexico, 87131-0001, USA
G. M. MKOJI
Affiliation:
Center for Biotechnology Research and Development, Kenya Medical Research Institute, Mbagathi Road, P.O. Box 54840-00200, City Square, Nairobi, Kenya
*
*Corresponding author: Department of Biology, University of New Mexico, MSC03 2020, Albuquerque, New Mexico, 87131-0001, USA. Tel: +505 2773174. Fax: +505 2770304. E-mail: bhanelt@unm.edu

Summary

Recent schistosomiasis control efforts in sub-Saharan Africa have focused nearly exclusively on treatment of humans with praziquantel. However, the extent to which wild mammals act as reservoirs for Schistosoma mansoni and therefore as sources of renewed transmission following control efforts is poorly understood. With the objective to study the role of small mammals as reservoir hosts, 480 animals belonging to 9 rodent and 1 insectivore species were examined for infection with schistosomes in Kisumu, in the Lake Victoria Basin, Kenya. Animals were collected from 2 sites: near the lakeshore and from Nyabera Marsh draining into the lake. A total of 6·0% of the animals captured, including 5 murid rodent species and 1 species of shrew (Crocidura olivieri) were infected with schistosomes. Four schistosome species were recovered and identified using cox1 DNA barcoding: S. mansoni, S. bovis, S. rodhaini and S. kisumuensis, the latter of which was recently described from Nyabera Marsh. Schistosoma mansoni and S. rodhaini were found infecting the same host individual (Lophuromys flavopunctatus), suggesting that this host species could be responsible for the production of hybrid schistosomes found in the area. Although the prevalence of S. mansoni infection in these reservoir populations was low (1·5%), given their potentially vast population size, their impact on transmission needs further study. Reservoir hosts could perpetuate snail infections and favour renewed transmission to humans once control programmes have ceased.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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

Allison, E. H. and Seeley, J. A. (2004). HIV and AIDS among fisherfolk: a threat to ‘responsible fisheries’? Fish and Fisheries 5, 215234.CrossRefGoogle Scholar
Arnold, M. L. (2004). Natural hybridization and the evolution of domesticated, pest, and disease organisms. Molecular Ecology 13, 997–1007.CrossRefGoogle ScholarPubMed
Arnold, M. L., Sapir, Y. and Martin, N. H. (2008). Genetic exchange and the origin of adaptations: prokaryotes to primates. Philosophical Transactions of the Royal Society, B 363, 28132820.CrossRefGoogle ScholarPubMed
Buhay, J. E. (2009). ‘COI-LIKE’ sequences are becoming problematic in molecular systematic and DNA barcoding studies. Journal of Crustacean Biology 29, 96–110.CrossRefGoogle Scholar
D'Andrea, P. S., Maroja, L. S., Gentile, R., Cerqueira, R., Maldonado, A. Jr. and Rey, L. (2000). The parasitism of Schistosoma mansoni (Digenea-Trematoda) in a naturally infected population of water rats, Nectomys squamipes (Rodentia-Sigmodontinae) in Brazil. Parasitology 120, 573582.CrossRefGoogle Scholar
D'Haenens, G. and Santele, A. (1955). Sur un cas humain de Schistosoma rodhaini trouve aux environs d' Elisabethville. Annales de la Societe Belge de Medecine Tropicale 35, 497.Google ScholarPubMed
Duplantier, J. M. and Sene, M. (2000). Rodents as reservoir hosts in the transmission of Schistosoma mansoni in Richard-Toll, Senegal, West Africa. Journal of Helminthology 74, 129135.CrossRefGoogle ScholarPubMed
Duplantier, J. M. and Sene, M. (2006). Rodents as definitive hosts of Schistosoma, with special reference to S. mansoni transmission. In Micromammals and Macroparasites: from Evolutionary Ecology to Management (ed. Morand, S., Krasnov, B. R. and Poulin, R.), pp. 527543. Springer, Tokyo, Japan.CrossRefGoogle Scholar
Fenwick, A., Webster, J. P., Bosque-Oliva, E., Blair, L., Fleming, F. M., Zhang, Y., Garba, A., Stothard, J. R., Gabrielli, A. F., Clements, A. C., Kabatereine, N. B., Toure, S., Dembele, R., Nyandindi, U., Mwansa, J. and Koukounari, A. (2009). The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002–2008. Parasitology 136, 17191730.CrossRefGoogle ScholarPubMed
Gentile, R., Costa-Neto, S. F., Goncalves, M. M., Bonecker, S. T., Fernandes, F. A., Garcia, J. S., Barreto, M. G., Soares, M. S., D'Andrea, P. S., Peralta, J. M. and Rey, L. (2006). An ecological field study of the water-rat Nectomys squamipes as a wild reservoir indicator of Schistosoma mansoni transmission in an endemic area. Memorias do Instituto Oswaldo Cruz 101, 111117.CrossRefGoogle Scholar
Granjon, L., Lavrenchenko, L., Corti, M., Coetzee, N. and Abdel Rahman, E. (2008). Mastomys natalensis. IUCN 2009. International Union for Conservation of Nature and Natural Resources Red List of Threatened Species. Version 2009.1, Cambridge, UK.Google Scholar
Handzel, T., Karanja, D. M., Addiss, D. G., Hightower, A. W., Rosen, D. H., Colley, D. G., Andove, J., Slutsker, L. and Secor, W. E. (2003). Geographic distribution of schistosomiasis and soil-transmitted helminths in western Kenya: implications for antihelminthic mass treatment. American Journal of Tropical Medicine and Hygiene 69, 318323.CrossRefGoogle ScholarPubMed
Hanelt, B., Brant, S. V., Steinauer, M. L., Maina, G. M., Kinuthia, J. M., Agola, L. E., Mwangi, I. N., Mungai, B. N., Mutuku, M. W., Mkoji, G. M. and Loker, E. S. (2009). Schistosoma kisumuensis n. sp. (Digenea: Schistosomatidae) from murid rodents in the Lake Victoria Basin, Kenya and its phylogenetic position within the S. haematobium species group. Parasitology 136, 987–1001.CrossRefGoogle Scholar
Isaacson, M. (1975). The ecology of Praomys (Mastomys) natalensis in southern Africa. Bulletin of the World Health Organization 52, 629636.Google ScholarPubMed
Karoum, K. O. and Amin, M. A. (1985). Domesticated and wild animals naturally infected with Schistosoma mansoni in the Gezira Irrigated Scheme, Sudan. Journal of Tropical Medicine and Hygiene 88, 8389.Google ScholarPubMed
Kawashima, K., Katamine, D., Sakamoto, M. and Shimada, M. (1978). Investigations on the role of wild rodents as reservoirs of human schistosomiasis in the Taveta area of Kenya, East Africa. Japanese Journal of Tropical Medicine and Hygiene 6, 195203.CrossRefGoogle Scholar
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.CrossRefGoogle ScholarPubMed
Kloos, H. (1985). Water resources development and schistosomiasis ecology in the Awash Valley, Ethiopia. Social Science and Medicine 20, 609625.CrossRefGoogle ScholarPubMed
Kuntz, R. E. (1958). Schistosoma sp. in shrews in Lower Egypt. Helminthological Society of Washington 25, 3740.Google Scholar
Kuntz, R. E. and Malakatis, G. M. (1955). Susceptibility studies in schistosomiasis. II. Susceptibility of wild mammals to infection by Schistosoma mansoni in Egypt, with emphasis on rodents. American Journal of Tropical Medicine and Hygiene 4, 7589.CrossRefGoogle ScholarPubMed
Lämmler, G. and Petranyi, G. (1971). Chemotherapeutic studies on experimental Schistosoma mansoni infection of Mastomys natalensis. Bulletin of the World Health Organization 44, 739750.Google ScholarPubMed
Lewis, F. (1998). Schistosomiasis. In Current Protocols in Immunology, Suppl. 28, Animal Models for Infectious Diseases (ed. Coligan, J. E., Kruisbeek, A. M., Margulies, D. H., Shevach, E. M. and Strober, W.),pp. 19.11.1119.11.28. John Wiley & Sons, Inc., New York, USA.Google Scholar
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. and Littlewood, D. T. (2003). The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126, 203224.CrossRefGoogle ScholarPubMed
Luttermoser, G. W. (1963). Infection of rodents with Schistosoma mansoni by ingestion of infected snails. Journal of Parasitology 49, 150.CrossRefGoogle ScholarPubMed
Makundi, R. H., Massawe, A. W. and Mulungu, L. S. (2007). Reproduction and population dynamics of Mastomys natalensis Smith, 1834 in an agricultural landscape in the Western Usambara Mountains, Tanzania. Integrative Zoology 2, 233238.CrossRefGoogle Scholar
McMahon, J. E. and Baalawy, S. S. (1967). A search for animal reservoirs of Schistosoma mansoni in the Mwanza area of Tanzania. East African Medical Journal 44, 325326.Google ScholarPubMed
Morgan, J. A., DeJong, R. J., Lwambo, N. J., Mungai, B. N., Mkoji, G. M. and Loker, E. S. (2003). First report of a natural hybrid between Schistosoma mansoni and S. rodhaini. Journal of Parasitology 89, 416418.CrossRefGoogle ScholarPubMed
Mungai, B. N., Agola, L. E., Morgan, J. A. T., DeJong, R. J., Karanja, D. M. S., Muchemi, G. M., Loker, E. S. and Mkoji, G. M. (2003). Schistosoma rodhaini in Kenya revisited. Proceedings of Workshop on African Freshwater Malacology, Kampala, Uganda, pp. 123132.Google Scholar
Nelson, G. (1983). Wild animals as reservoir hosts of parasitic disease of man in Kenya. In Tropical Parasitoses and Parasitic Zoonoses (ed. Dunsmore, J. D.), pp. 5972. World Association for the Advancement of Veterinary Parasitology, Perth, Australia.Google Scholar
Nelson, G. S. (1960). Schistosome infections as zoonoses in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 54, 301316.CrossRefGoogle ScholarPubMed
Nelson, G. S., Teesdale, C. and Highton, R. B. (1962). The role of animals as reservoirs of bilharziasis in Africa. In Bilharziasis (ed. Wolstenholme, G. E. W. and O'Connor, M.), pp. 127149. Ciba Foundation, London, UK.Google Scholar
Ouma, J. H. and Fenwick, A. (1991). Animal reservoirs of schistosomiasis. In Parasitic Helminths and Zoonoses in Africa (ed. Macpherson, C. N. L. and Craig, P. S.), pp. 224236. Unwin Hyman, London, UK.Google Scholar
Pitchford, R. J. (1959). Natural schistosome infection in South African rodents. Transactions of the Royal Society of Tropical Medicine and Hygiene 53, 213.CrossRefGoogle Scholar
Pitchford, R. J. (1977). A check list of definitive hosts exhibiting evidence of the genus Schistosoma Weinland, 1858 acquired naturally in Africa and the Middle East. Journal of Helminthology 51, 229252.CrossRefGoogle ScholarPubMed
Pitchford, R. J. and Visser, P. S. (1962). The role of naturally infected wild rodents in the epidemiology of schistosomiasis in the eastern Transvaal. Transactions of the Royal Society of Tropical Medicine and Hygiene 56, 126135.CrossRefGoogle ScholarPubMed
Prugnolle, F., De Meeus, T., Durand, P., Sire, C. and Théron, A. (2002). Sex-specific genetic structure in Schistosoma mansoni: evolutionary and epidemiological implications. Molecular Ecology 11, 12311238.CrossRefGoogle ScholarPubMed
Rey, L. (1993). Non-human vertebrate hosts of Schistosoma mansoni and schistosomiasis transmission in Brazil. Research and Reviews for Parasitology 53, 1325.Google Scholar
Rodrigues-Silva, R., Machado e Silva, J. R., Faerstein, N. F., Lenzi, H. L. and Rey, L. (1992). Natural infection of wild rodents by Schistosoma mansoni. Parasitological aspects. Memorias do Instituto Oswaldo Cruz 87, 271276.CrossRefGoogle Scholar
Saoud, M. F. (1966). On the morphology of Schistosoma rodhaini from Kenya. Journal of Helminthology 40, 147154.CrossRefGoogle ScholarPubMed
Schwetz, J. (1954). On two schistosomes of wild rodents of the Belgian Congo: Schistosoma rodhaini Brumpt, 1931; and Schistosoma mansoni var rodentorum Schwetz, 1953; and their relationship to S. mansoni of man. Transactions of the Royal Society of Tropical Medicine and Hygiene 48, 89–100.CrossRefGoogle Scholar
Schwetz, J. (1956). Role of wild rats and domestic rats (Rattus rattus) in schistosomiasis in man. Transactions of the Royal Society of Tropical Medicine and Hygiene 50, 275282.CrossRefGoogle Scholar
Sire, C., Durand, P., Pointier, J. P. and Théron, A. (1999). Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplified polymorphic DNA markers. Journal of Parasitology 85, 436441.CrossRefGoogle Scholar
Sluydtsa, V., Davisa, S., Mercelisa, S. and Leirsa, H. (2009). Comparison of multimammate mouse (Mastomys natalensis) demography in monoculture and mosaic agricultural habitat: implications for pest management. Crop Protection 28, 647654.CrossRefGoogle Scholar
Steinauer, M. L., Agola, L. E., Mwangi, I. N., Mkoji, G. M. and Loker, E. S. (2008 b). Molecular epidemiology of Schistosoma mansoni: a robust, high-throughput method to assess multiple microsatellite markers from individual miracidia. Infection, Genetics and Evolution 8, 6873.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Hanelt, B., Mwangi, I. N., Maina, G. M., Agola, L. E., Kinuthia, J. M., Mutuku, M. W., Mungai, B. N., Wilson, W. D., Mkoji, G. M. and Loker, E. S. (2008 c). Introgressive hybridization of human and rodent schistosome parasites in western Kenya. Molecular Ecology 17, 50625074.CrossRefGoogle ScholarPubMed
Steinauer, M., Mwangi, I., Maina, G., Kinuthia, J., Mutuku, M., Agola, E., Mungai, B., Mkoji, G. and Loker, E. S. (2008 a). Interactions between natural populations of human and rodent schistosomes in the Lake Victoria region of Kenya: a molecular epidemiological approach. PLoS Neglected Tropical Diseases 16, e222.CrossRefGoogle Scholar
Stijns, J. (1952). Sur les rogeurs hôtes naturals de Schistosoma rodhaini Brumpt. Annales de Parasitologie Humaine et Comparée 27, 385386.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, 15961599.CrossRefGoogle ScholarPubMed
Théron, A. (1984). Early and late shedding patterns of Schistosoma mansoni cercariae: ecological significance in transmission to human and murine hosts. Journal of Parasitology 70, 652655.CrossRefGoogle ScholarPubMed
Théron, A. and Pointier, J. P. (1995). Ecology, dynamics, genetics and divergence of trematode populations in heterogeneous environments: the model of Schistosoma mansoni in the insular focus of Guadeloupe. Research and Reviews for Parasitology 55, 4964.Google Scholar
Théron, A., Pointier, J. P., Morand, S., Imbert-Establet, D. and Borel, G. (1992). Long-term dynamics of natural populations of Schistosoma mansoni among Rattus rattus in patchy environment. Parasitology 104, 291298.CrossRefGoogle ScholarPubMed
Truett, G. E., Heeger, P., Mynatt, R. L., Truett, A. A., Walker, J. A. and Warman, M. L. (2000). Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). BioTechniques 29, 5254.CrossRefGoogle ScholarPubMed