Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-18T02:45:37.269Z Has data issue: false hasContentIssue false

Field survey for strongyloidiasis in eastern Uganda with observations on efficacy of preventive chemotherapy and co-occurrence of soil-transmitted helminthiasis/intestinal schistosomiasis

Published online by Cambridge University Press:  20 October 2010

J.C. Sousa-Figueiredo
Affiliation:
WHO Collaborating Centre Schistosomiasis, Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, LondonSW7 5BD, United Kingdom Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, LondonWC1E 7HT, United Kingdom
M. Day
Affiliation:
Faculty of Medicine, University of Dundee, Nethergate, DundeeDD1 4HH, United Kingdom
M. Betson
Affiliation:
WHO Collaborating Centre Schistosomiasis, Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, LondonSW7 5BD, United Kingdom
C. Rowell
Affiliation:
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
A. Wamboko
Affiliation:
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
M. Arinaitwe
Affiliation:
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
F. Kazibwe
Affiliation:
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
N.B. Kabatereine
Affiliation:
Vector Control Division, Ministry of Health, P.O. Box 1661, Kampala, Uganda
J.R. Stothard*
Affiliation:
WHO Collaborating Centre Schistosomiasis, Wolfson Wellcome Biomedical Laboratories, Department of Zoology, Natural History Museum, LondonSW7 5BD, United Kingdom

Abstract

Following our previous field surveys for strongyloidiasis in western Uganda, 120 mothers and 232 children from four villages in eastern Uganda were examined, with two subsequent investigative follow-ups. As before, a variety of diagnostic methods were used: Baermann concentration, Koga agar plate and strongyloidid enzyme-linked immunosorbent assay (ELISA), as well as Kato–Katz faecal smears for detection of eggs of other helminths. At baseline, the general prevalence of Strongyloides stercoralis was moderate: 5.4% as estimated by Baermann and Koga agar methods combined. A much higher estimate was found by ELISA (42.3%) which, in this eastern setting, appeared to be confounded by putative cross-reaction(s) with other nematode infections. Preventive chemotherapy using praziquantel and albendazole was offered to all participants at baseline. After 21 days the first follow-up was conducted and ‘cure rates’ were calculated for all parasites encountered. Eleven months later, the second follow-up assessed longer-term trends. Initial treatments had little, if any, effect on S. stercoralis, and did not alter local prevalence, unlike hookworm infections and intestinal schistosomiasis. We propose that geographical patterns of strongyloidiasis are likely not perturbed by ongoing praziquantel/albendazole campaigns. Antibody titres increased after the first follow-up then regressed towards baseline levels upon second inspection. To better define endemic areas for S. stercoralis, careful interpretation of the ELISA is warranted, especially where diagnosis is likely being confounded by polyparasitism and/or other treatment regimens; new molecular screening tools are clearly needed.

Type
Research Papers
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

Agrawal, V., Agarwal, T. & Ghoshal, U.C. (2009) Intestinal strongyloidiasis: a diagnosis frequently missed in the tropics. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 242246.CrossRefGoogle ScholarPubMed
Appleton, C.C., Maurihungirire, M. & Gouws, E. (1999) The distribution of helminth infections along the coastal plain of Kwazulu-Natal province, South Africa. Annals of Tropical Medicine and Parasitology 93, 859868.CrossRefGoogle ScholarPubMed
Bennett, A. & Guyatt, H.L. (2000) Reducing intestinal nematode infection: efficacy of albendazole and mebendazole. Parasitology Today 16, 7174.CrossRefGoogle ScholarPubMed
Brooker, S., Whawell, S., Kabatereine, N.B., Fenwick, A. & Anderson, R.M. (2004) Evaluating the epidemiological impact of national control programmes for helminths. Trends in Parasitology 20, 537545.Google Scholar
Dreyer, G., Fernandes-Silva, E., Alves, S., Rocha, A., Albuquerque, R. & Addiss, D. (1996) Patterns of detection of Strongyloides stercoralis in stool specimens: implications for diagnosis and clinical trials. Journal of Clinical Microbiology 34, 25692571.Google Scholar
Glickman, L.T., Camara, A.O., Glickman, N.W. & McCabe, G.P. (1999) Nematode intestinal parasites of children in rural Guinea, Africa: prevalence and relationship to geophagia. International Journal of Epidemiology 28, 169174.CrossRefGoogle ScholarPubMed
Handzel, T., Karanja, D.M.S., Addiss, D.G., Hightower, A.W., Rosen, D.H., Colley, D.G., Andove, J., Slutsker, L. & Secor, W.E. (2003) Geographic distribution of schistosomiasis and soil-transmitted helminths in Western Kenya: implications for anthelminthic mass treatment. American Journal of Tropical Medicine and Hygiene 69, 318323.CrossRefGoogle ScholarPubMed
Harper, R. & Reeves, B. (1999) Reporting of precision of estimates for diagnostic accuracy: a review. British Medical Journal 318, 13221323.CrossRefGoogle ScholarPubMed
Hernandez-Chavarria, F. & Avendano, L. (2001) A simple modification of the Baermann method for diagnosis of strongyloidiasis. Memorias do Instituto Oswaldo Cruz 96, 805807.CrossRefGoogle ScholarPubMed
Johansen, M.V., Sacko, M., Vennervald, B.J. & Kabatereine, N.B. (2007) Leave children untreated and sustain inequity! Trends in Parasitology 23, 568569.Google Scholar
Kabatereine, N.B., Kemijumbi, J., Kazibwe, F. & Onapa, A.W. (1997) Human intestinal parasites in primary school children in Kampala, Uganda. East Africa Medical Journal 74, 311314.Google Scholar
Katz, N., Chavez, A. & Pellegrino, J. (1972) A simple device for quantitative stool thicksmear technique in schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de São Paulo 14, 397400.Google Scholar
Keiser, J. & Utzinger, J. (2008) Efficacy of current drugs against soil-transmitted helminth infections – systematic review and meta-analysis. Journal of the American Medical Association 299, 19371948.Google Scholar
Knopp, S., Mohammed, K.A., Rollinson, D., Stothard, J.R., Khamis, I.S., Utzinger, J. & Marti, H. (2009) Changing patterns of soil-transmitted helminthiases in Zanzibar in the context of national helminth control programs. American Journal of Tropical Medicine and Hygiene 81, 10711078.Google Scholar
Koga, K., Kasuya, S., Khamboonruang, C., Sukhavat, K., Ieda, M., Takatsuka, N., Kita, K. & Ohtomo, H. (1991) A modified agar plate method for detection of Strongyloides stercoralis. American Journal of Tropical Medicine and Hygiene 45, 518521.Google Scholar
Kolaczinski, J.H., Kabatereine, N.B., Onapa, A.W., Ndyomugyenyi, R., Kakembo, A.S. & Brooker, S. (2007) Neglected tropical diseases in Uganda: the prospect and challenge of integrated control. Trends in Parasitology 23, 485493.CrossRefGoogle ScholarPubMed
Lindo, J.F., Atkins, N.S., Lee, M.G., Robinson, R.D. & Bundy, D.A. (1996) Parasite-specific serum IgG following successful treatment of endemic strongyloidiasis using ivermectin. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 702703.CrossRefGoogle ScholarPubMed
Liu, L.X. & Weller, P.F. (1993) Strongyloidiasis and other intestinal nematode infections. Infectious Disease Clinics of North America 7, 655682.CrossRefGoogle ScholarPubMed
Marti, H. & Koella, J.C. (1993) Multiple stool examinations for ova and parasites and rate of false-negative results. Journal of Clinical Microbiology 31, 30443045.CrossRefGoogle ScholarPubMed
Muhangi, L., Woodburn, P., Omara, M., Ornoding, N., Kizito, D., Mpairwe, H., Nabulime, J., Ameke, C., Morison, L.A. & Elliott, A.M. (2007) Associations between mild-to-moderate anaemia in pregnancy and helminth, malaria and HIV infection in Entebbe, Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 899907.Google Scholar
Nielsen, P.B. & Mojon, M. (1987) Improved diagnosis of Strongyloides stercoralis by seven consecutive stool specimens. Zentralblatt für Bakteriologie, Mikrobiologie, und Hygiene Series A 263, 616618.CrossRefGoogle ScholarPubMed
Olsen, A., van Lieshout, L., Marti, H., Polderman, T., Polman, K., Steinmann, P., Stothard, R., Thybo, S., Verweij, J.J. & Magnussen, P. (2009) Strongyloidiasis – the most neglected of the neglected tropical diseases? Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 967972.CrossRefGoogle ScholarPubMed
Onapa, A.W., Simonsen, P.E., Baehr, I. & Pedersen, E.M. (2005a) Rapid assessment of the geographical distribution of lymphatic filariasis in Uganda, by screening of schoolchildren for circulating filarial antigens. Annals of Tropical Medicine and Parasitology 99, 141153.CrossRefGoogle ScholarPubMed
Onapa, A.W., Simonsen, P.E., Baehr, I. & Pedersen, E.M. (2005b) Rapid assessment of the geographical distribution of Mansonella perstans infections in Uganda, by screening schoolchildren for microfilariae. Annals of Tropical Medicine and Parasitology 99, 383393.CrossRefGoogle ScholarPubMed
Siddiqui, A.A. & Berk, S.L. (2001) Diagnosis of Strongyloides stercoralis infection. Clinical Infectious Diseases 33, 10401047.CrossRefGoogle ScholarPubMed
Sousa-Figueiredo, J.C., Pleasant, J., Day, M., Betson, M., Rollinson, D., Montresor, A., Kazibwe, F., Kabatereine, N. & Stothard, J.R. (2010) Treatment of intestinal schistosomiasis in Ugandan preschool children: best diagnosis, treatment efficacy and side-effects, and an extended praziquantel dosing pole. International Health 2, 103113.Google Scholar
Speare, R. & Durrheim, D. (2004) Mass treatment with ivermectin: an underutilized public health strategy. Bulletin of the World Health Organization 82, 562.Google Scholar
Steinmann, P., Zhou, X.N., Du, Z.W., Jiang, J.Y., Wang, L.B., Wang, X.Z., Li, L.H., Marti, H. & Utzinger, J. (2007) Occurrence of Strongyloides stercoralis in Yunnan Province, China, and comparison of diagnostic methods. PLoS Neglected Tropical Diseases 1, e75.CrossRefGoogle ScholarPubMed
Stothard, J.R. & Gabrielli, A.F. (2007a) Response to Johansen et al. Leave children untreated and sustain inequity! Trends in Parasitology 23, 569570.CrossRefGoogle Scholar
Stothard, J.R. & Gabrielli, A.F. (2007b) Schistosomiasis in African infants and preschool children: to treat or not to treat? Trends in Parasitology 23, 8386.Google Scholar
Stothard, J.R., Pleasant, J., Oguttu, D., Adriko, M., Galimaka, R., Ruggiana, A., Kazibwe, F. & Kabatereine, N.B. (2008) Strongyloides stercoralis: a field-based survey of mothers and their preschool children using ELISA, Baermann and Koga plate methods reveals low endemicity in western Uganda. Journal of Helminthology 82, 263269.Google Scholar
Sudarshi, S., Stumpfle, R., Armstrong, M., Ellman, T., Parton, S., Krishnan, P., Chiodini, P.L. & Whitty, C.J. (2003) Clinical presentation and diagnostic sensitivity of laboratory tests for Strongyloides stercoralis in travellers compared with immigrants in a non-endemic country. Tropical Medicine & International Health 8, 728732.CrossRefGoogle Scholar
van Doorn, H.R., Koelewijn, R., Hofwegen, H., Gilis, H., Wetsteyn, J.C., Wismans, P.J., Sarfati, C., Vervoort, T. & van Gool, T. (2007) Use of enzyme-linked immunosorbent assay and dipstick assay for detection of Strongyloides stercoralis infection in humans. Journal of Clinical Microbiology 45, 438442.CrossRefGoogle ScholarPubMed
Verweij, J.J., Canales, M., Polman, K., Ziem, J., Brienen, E.A., Polderman, A.M. & van Lieshout, L. (2009) Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 342346.Google Scholar
WHO (2002) Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Report of a WHO Expert Committee. Geneva, World Health Organization.Google Scholar
WHO (2008) Soil-transmitted helminthiasis. Weekly epidemiological record no. 83. Geneva, World Health Organization.Google Scholar
Woywodt, A. & Kiss, A. (2002) Geophagia: the history of earth-eating. Journal of the Royal Society of Medicine 95, 143146.CrossRefGoogle ScholarPubMed