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Intestinal schistosomiasis in chimpanzees on Ngamba Island, Uganda: observations on liver fibrosis, schistosome genetic diversity and praziquantel treatment

Published online by Cambridge University Press:  25 October 2012

Ecology & Evolutionary Biology, Princeton University, Princeton, New Jersey 08544, USA
College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, P.O. Box 7062, Kampala, Uganda Conservation & Ecosystem Health Alliance (CEHA), P.O. Box 34153, Kampala, Uganda
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
Chimpanzee Sanctuary and Wildlife Conservation Trust (CSWCT), Entebbe, Uganda
Chimpanzee Sanctuary and Wildlife Conservation Trust (CSWCT), Entebbe, Uganda
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda Department of Radiology, Mulago Hospital, P.O. Box 7051, Kampala, Uganda
Disease Control Strategy Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
Disease Control Strategy Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK
*Corresponding author: Disease Control Strategy Group, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK. E-mail:


Despite treatment with praziquantel (PZQ) at 40 mg/kg in food, several chimpanzees on Ngamba Island Chimpanzee Sanctuary (NICS) continue to excrete eggs of Schistosoma mansoni. To monitor disease, 8 animals were closely examined under anaesthesia in March 2011 with portable ultrasonography and by rectal snip biopsy. Schistosome genetic diversity had been previously assayed within 4 of these chimpanzees, finding extensive diversity with 27 DNA barcodes encountered, although none was common to all animals. Calcified schistosome eggs were found in the rectal snips from 5 chimpanzees and liver fibrosis was clearly documented, indicative of progressive disease in 6 animals, the latter being surprisingly advanced in a younger chimpanzee. All 8 animals were treated under anaesthesia by oral gavage with PZQ at 60 mg/kg dosing that was well tolerated. These animals were again re-examined in June 2012 using stool and urine sampling. Only 1 chimpanzee appeared to be free from infection and active egg excretion was confirmed in 6 animals. If intestinal schistosomiasis is to be controlled within this setting, a long-term disease management plan is required which should combine active case-detection with an insistent treatment regime with praziquantel for these chimpanzees, exploring perhaps the performance of even higher dosing.

Research Article
Copyright © Cambridge University Press 2012

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Balen, J., Stothard, J. R., Kabatereine, N. B., Tukahebwa, E. M., Kazibwe, F., Whawell, S., Webster, J. P., Utzinger, J. and Fenwick, A. (2006). Morbidity due to Schistosoma mansoni: an epidemiological assessment of distended abdomen syndrome in Ugandan school children with observations before and 1-year after anthelminthic chemotherapy. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 10391048.CrossRefGoogle ScholarPubMed
Clements, A. C. A., Deville, M.-A., Ndayishimiye, O., Brooker, S. and Fenwick, A. (2010). Spatial co-distribution of neglected tropical diseases in the East African Great Lakes region: revisiting the justification for integrated control. Tropical Medicine & International Health 15, 198207.CrossRefGoogle ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2005). Effective sizes of macroparasite populations: a conceptual model. Trends in Parasitology 21, 212217.CrossRefGoogle ScholarPubMed
Eberl, M., Langermans, J. A. M., Frost, P. A., Vervenne, R. A., van Dam, G. J., Dellder, A. M., Thomas, A. W., Coulson, P. A. and Wilson, A. (2001). Cellular and humoral responses and protection against schistosomes induced by a radiation-attentuated vaccine in chimpanzees. Infection and Immunity 69, 53525362.CrossRefGoogle ScholarPubMed
Gower, C., Shrivastava, J., Lamerton, P., Rollinson, D., Webster, B., Emery, A., Kabatereine, N. and Webster, J. (2007). Development and application of an ethically and epidemiologically advantageous assay for the multi-locus microsatellite analysis of Schistosoma mansoni. Parasitology 134, 523536.CrossRefGoogle ScholarPubMed
Katz, N., Chaves, A. and Pellegrino, J. (1972). A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Revista Instituto de Medicina Tropical de Sao Paulo 14, 397400.Google ScholarPubMed
Khalil, H. M., Abdel-Baki, M. H. A. M. M., Saleh, S. M., Abbas, M. M. and Amir, E. A. (1993). Evaluation of direct and indirect methods in diagnosis of chronic intetsinal schistosomiasis in Menoufia Governorate. Journal of the Egyptian Society of Parasitology 23, 555561.Google Scholar
King, C. H., Magak, P., Salam, E. A., Ouma, J. H., Kariuki, H. C. and Blanton, R. E. (2003). Measuring morbidity in schistosomiasis mansoni: relationship between image pattern, portal vein diameter and portal branch thickness in large-scale surveys using new WHO coding guidelines for ultrasound in schistosomiasis. Tropical Medicine & International Health 8, 109117.CrossRefGoogle ScholarPubMed
Morgan, J. A. T., Dejong, R. J., Adeoye, G. O., Ansa, E. D. O., Barbosa, C. S., Bremond, P., Cesari, I. M., Charbonnel, N., Correa, L. R., Coulibaly, G., D'Andrea, P. S., De Souza, C. P., Doenhoff, M. J., File, S., Idris, M. A., Incani, R. N., Jarne, P., Karanja, D. M. S., Kazibwe, F., Kpikpi, J., Lwambo, N. J. S., Mabaye, A., Magalhaes, L. A., Makundi, A., Mone, H., Mouahid, G., Muchemi, G. M., Mungai, B. N., Sene, M., Southgate, V., Tchuente, L. A. T., Theron, A., Yousif, F., Magalhaes, E. M. Z., Mkoji, G. M. and Loker, E. S. (2005). Origin and diversification of the human parasite Schistosoma mansoni. Molecular Ecology 14, 38893902.CrossRefGoogle ScholarPubMed
Standley, C. J., Adriko, M., Alinaitwe, M., Kazibwe, F., Kabatereine, N. B. and Stothard, J. R. (2009). Intestinal schistosomiasis and soil-transmitted helminthiasis in Ugandan schoolchildren: a rapid mapping assessment. Geospatial Health 4, 3953.CrossRefGoogle ScholarPubMed
Standley, C. J., Kabatereine, N. B., Lange, C., Lwambo, N. J. S. and Stothard, J. R. (2010). Molecular epidemiology and phylogeography of Schistosoma mansoni around Lake Victoria. Parasitology 137, 19371949.CrossRefGoogle ScholarPubMed
Standley, C. J., Mugisha, L., Verweij, J. J., Adriko, M., Arinaitwe, M., Rowell, C., Atuhaire, A., Betson, M., Hobbs, E., Tulleken, C. R. V., Kane, R. A., Lieshout, L. V., Ajarova, L., Kabatereine, N. B. and Stothard, J. R. (2011). Confirmed infection with intestinal schistosomiasis in semi-captive wild born chimpanzees on Ngamba Island, Uganda Vector Borne and Zoonotic Diseases 11, 169176.CrossRefGoogle ScholarPubMed
Standley, C. J., Mugisha, L., Dobson, A. P. and Stothard, J. R. (2012 a). Zoonotic schistosomiasis in non-human primates: past, present and future activities at the human-wildlife interface in Africa. Journal of Helminthology 86, 131140.CrossRefGoogle ScholarPubMed
Standley, C. J. and Stothard, J. R. (2010). Towards defining appropriate strategies for targeted NTD control. Tropical Medicine & International Health 15, 772773.CrossRefGoogle ScholarPubMed
Standley, C. J., Vounatsou, P., Gosoniu, L., Mckeon, C., Adriko, M., Kabatereine, N. B. and Stothard, J. R. (2012 b). Micro-scale environmental determinants of intestinal schistosomiasis transmission biology on Ngamba and Kimi Islands, Lake Victoria, Uganda: Spatial modelling, molluscan diversity analysis and population genetics. Acta Tropica (in the Press).Google Scholar
Steinauer, M. L., Blouin, M. S. and Criscione, C. D. (2010). Applying evolutionary genetics to schistosome epidemiology. Infection, Genetics and Evolution 10, 433443.CrossRefGoogle ScholarPubMed
Stothard, J. R., Mugisha, L. and Standley, C. J. (2012). Stopping schistosomes from ‘monkeying-around’ in chimpanzees. Trends in Parasitology 28, 320326.CrossRefGoogle ScholarPubMed
Stothard, J. R. and Rollinson, D. (1997). Partial DNA sequences from the mitochondrial cytochrome oxidase subunit I (COI) gene can differentiate the intermediate snail hosts Bulinus globosus and B. nasutus (Gastropoda: Planorbidae). Journal of Natural History 31, 727737.CrossRefGoogle Scholar
Stothard, J. R., Webster, B. L., Weber, T., Nyakaana, S., Webster, J. P., Kazibwe, F., Kabatereine, N. B. and Rollinson, D. (2009). Molecular epidemiology of Schistosoma mansoni in Uganda: DNA barcoding reveals substantial genetic diversity within Lake Albert and Lake Victoria populations. Parasitology 136, 18131824.CrossRefGoogle Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution 28, 27312739.CrossRefGoogle ScholarPubMed
Webster, B. L., Webster, J. P., Gouvras, A. N., Garba, A., Lamine, M. S., Diaw, O. T., Seye, M. M., Tuchuem-Tchuente, L. A., Simoonga, Mulbila, L., Mwanga, J., Lwambo, N. J. S., Kabatereine, N. B., Lange, C. N., Kariuki, C., Mkoji, G., Rollinson, D., Stothard, J. R. (2012). DNA ‘barcoding’ of Schistosoma mansoni across sub-Saharan Africa supports substantial within local diversity and geographical separation of genotypes. Acta Tropica (in the Press).Google Scholar