Hostname: page-component-848d4c4894-x5gtn Total loading time: 0 Render date: 2024-06-01T04:05:23.894Z Has data issue: false hasContentIssue false

Effect of sampling and diagnostic effort on the assessment of schistosomiasis and soil-transmitted helminthiasis and drug efficacy: a meta-analysis of six drug efficacy trials and one epidemiological survey

Published online by Cambridge University Press:  14 April 2014

BRUNO LEVECKE*
Affiliation:
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
SIMON J. BROOKER
Affiliation:
Department of Disease Control, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 7HT, UK
STEFANIE KNOPP
Affiliation:
Wolfson Wellcome Biomedical Laboratories, Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Socinstrasse 57, CH-4002 Basel, Switzerland University of Basel, Petersplatz 1, CH-4003 Basel, Switzerland
PETER STEINMANN
Affiliation:
Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Socinstrasse 57, CH-4002 Basel, Switzerland University of Basel, Petersplatz 1, CH-4003 Basel, Switzerland
JOSE CARLOS SOUSA-FIGUEIREDO
Affiliation:
Department of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, Keppel Street, London WC1E 6HT, UK
J. RUSSELL STOTHARD
Affiliation:
Department of Parasitology, Liverpool School of Tropical Medicine, Liverpool L3 5QA, UK
JÜRG UTZINGER
Affiliation:
Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Socinstrasse 57, CH-4002 Basel, Switzerland University of Basel, Petersplatz 1, CH-4003 Basel, Switzerland
JOZEF VERCRUYSSE
Affiliation:
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
*
*Corresponding author: Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium. E-mail: Bruno.Levecke@UGent.be

Summary

It is generally recommended to perform multiple stool examinations in order to improve the diagnostic accuracy when assessing the impact of mass drug administration programmes to control human intestinal worm infections and determining efficacy of the drugs administered. However, the collection and diagnostic work-up of multiple stool samples increases costs and workload. It has been hypothesized that these increased efforts provide more accurate results when infection and drug efficacy are summarized by prevalence (proportion of subjects infected) and cure rate (CR, proportion of infected subjects that become egg-negative after drug administration), respectively, but not when these indicators are expressed in terms of infection intensity and egg reduction rate (ERR). We performed a meta-analysis of six drug efficacy trials and one epidemiological survey. We compared prevalence and intensity of infection, CR and ERR based on collection of one or two stool samples that were processed with single or duplicate Kato-Katz thick smears. We found that the accuracy of prevalence estimates and CR was lowest with the minimal sampling effort, but that this was not the case for estimating infection intensity and ERR. Hence, a single Kato-Katz thick smear is sufficient for reporting infection intensity and ERR following drug treatment.

Type
Special Issue Article
Copyright
Copyright © Cambridge University Press 2014 

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

Albonico, M., Ame, S. M., Vercruysse, J. and Levecke, B. (2012). Comparison of Kato-Katz thick smear and McMaster egg counting method for monitoring drug efficacy against soil-transmitted helminths in school children of Pemba Island, Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 107, 199201.Google Scholar
Albonico, M., Rinaldi, L., Sciascia, S., Morgoglione, M. E., Piemonte, M., Maurelli, M. P., Musella, V., Utzinger, J., Ali, S. M. and Cringoli, G. (2013). Comparison of three copromicroscopic methods to assess albendazole efficacy against soil-transmitted helminth infections in school-aged children on Pemba Island. Transactions of the Royal Society of Tropical Medicine and Hygiene 107, 493501.CrossRefGoogle ScholarPubMed
Anderson, R., Hollingsworth, T. D., Truscott, J. and Brooker, S. (2012). Optimisation of mass chemotherapy to control soil-transmitted helminth infection. Lancet 379, 289290.Google Scholar
Bergquist, R., Johansen, M. V. and Utzinger, J. (2009). Diagnostic dilemmas in helminthology: what tools to use and when? Trends in Parasitology 25, 151156.Google Scholar
Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Loukas, A., Diemert, D. and Hotez, P. J. (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367, 15211532.Google Scholar
Booth, M., Vounatsou, P., N'Goran, E. K., Tanner, M. and Utzinger, J. (2003). The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma mansoni and hookworm co-infections in rural Côte d'Ivoire. Parasitology 127, 525531.CrossRefGoogle ScholarPubMed
Brooker, S., Hotez, P. J. and Bundy, D. A. P. (2010). The global atlas of helminth infection: mapping the way forward in neglected tropical disease control. PLoS Neglected Tropical Diseases 4, e779.Google Scholar
Brooker, S. J., Pullan, R. L., Gitonga, C. W., Ashton, R. A., Kolaczinski, J. H., Kabatereine, N. B. and Snow, R. W. (2012). Plasmodium–helminth coinfection and its sources of heterogeneity across East Africa. Journal of Infectious Diseases 205, 841852.Google Scholar
Colley, D. G., Binder, S., Campbell, C., King, C. H., Tchuem Tchuenté, L.-A., N'Goran, E. K., Erko, B., Karanja, D. M., Kabatereine, N. B., van Lieshout, L. and Rathbun, S. (2013). A five-country evaluation of a point-of-care circulating cathodic antigen urine assay for the prevalence of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 88, 426432.Google Scholar
Cringoli, G., Rinaldi, L., Maurelli, M. P. and Utzinger, J. (2010). FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nature Protocols 5, 503515.Google Scholar
Danso-Appiah, A., Olliaro, P. L., Donegan, S., Sinclair, D. and Utzinger, J. (2013). Drugs for treating Schistosoma mansoni infection. Cochrane Database Systematic Reviews 2, CD000528.Google Scholar
Engels, D., Sinzinkayo, E. and Gryseels, B. (1996). Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications. American Journal of Tropical Medicine and Hygiene 54, 319324.Google Scholar
Engels, D., Sinzinkayo, E., de Vlas, S. J. and Gryseels, B. (1997). Intraspecimen fecal egg count variation in Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene 57, 571577.Google Scholar
Glinz, D., Silué, K. D., Knopp, S., Lohourignon, K. L., Yao, P. K., Steinmann, P., Rinaldi, L., Cringoli, G., N'Goran, E. K. and Utzinger, J. (2010). Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Neglected Tropical Diseases 4, e754.Google Scholar
Hotez, P. J., Molyneux, D. H., Fenwick, A., Kumaresan, J., Ehrlich Sachs, S., Sachs, J. D. and Savioli, L. (2007). Control of neglected tropical diseases. New England Journal of Medicine 357, 10181027.Google Scholar
Humphries, D., Mosites, E., Otchere, J., Twum, W. A., Woo, L., Jones-Sanpei, H., Harrison, L. M., Bungiro, R. D., Benham-Pyle, B., Bimi, L., Edoh, D., Bosompem, K., Wilson, M. and Cappello, M. (2011). Epidemiology of hookworm infection in Kintampo North Municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure. American Journal of Tropical Medicine and Hygiene 84, 792800.CrossRefGoogle ScholarPubMed
Hürlimann, E., Schur, N., Boutsika, K., Stensgaard, A.-S., Laserna de Himpsl, M., Ziegelbauer, K., Laizer, N., Camenzind, L., Di Pasquale, A., Ekpo, U. F., Simoonga, C., Mushinge, G., Saamak, C. F. L., Utzinger, J., Kristensen, T. K. and Vounatsou, P. (2011). Toward an open-access global database for mapping, control, and surveillance of neglected tropical diseases. PLoS Neglected Tropical Disease 5, e1404.CrossRefGoogle ScholarPubMed
Jeandron, A., Abdyldaieva, G., Usubalieva, J., Ensink, J. H. J., Cox, J., Matthys, B., Rinaldi, L., Cringoli, G. and Utzinger, J. (2010). Accuracy of the Kato-Katz, adhesive tape and FLOTAC techniques for helminth diagnosis among children in Kyrgyzstan. Acta Tropica 116, 185192.Google Scholar
Katz, N., Chaves, A. and Pellegrino, J. (1972). A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Revista do Instituto de Medicina Tropical São Paulo 14, 397400.Google Scholar
Keiser, J. and Utzinger, J. (2008). Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. Journal of American Medical Association 299, 19371948.Google Scholar
Knopp, S., Mgeni, A. F., Khamis, I. S., Steinmann, P., Stothard, J. R., Rollinson, D., Marti, H. and Utzinger, J. (2008). Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Neglected Tropical Diseases 2, e331.CrossRefGoogle ScholarPubMed
Knopp, S., Glinz, D., Rinaldi, L., Mohammed, K. A., N'Goran, E. K., Stothard, J. R., Marti, H., Cringoli, G., Rollinson, D. and Utzinger, J. (2009). FLOTAC: a promising technique for detecting helminth eggs in human feces. Transactions of the Royal Society of Tropical Medicine Hygiene 103, 11901194.Google Scholar
Knopp, S., Mohammed, K. A., Speich, B., Hattendorf, J., Khamis, I. S., Khamis, A. N., Stothard, J. R., Rollinson, D., Marti, H. and Utzinger, J. (2010). Albendazole and mebendazole administered alone or in combination with ivermectin against Trichuris trichiura: a randomized controlled trial. Clinical Infectious Diseases 51, 14201428.Google Scholar
Knopp, S., Speich, B., Hattendorf, J., Rinaldi, L., Mohammed, K. A., Khamis, I. S., Mohamemed, A. S., Albonico, M., Rollinson, D., Marti, H., Cringoli, G. and Utzinger, J. (2011). Diagnostic accuracy of Kato-Katz and FLOTAC for assessing anthelmintic drug efficacy. PLoS Neglected Tropical Diseases 5, e1036.Google Scholar
Knopp, S., Steinmann, P., Keiser, J. and Utzinger, J. (2012). Nematode infections: soil-transmitted helminths and trichinella. Infectious Disease Clinics North America 26, 341358.CrossRefGoogle ScholarPubMed
Krauth, S. J., Coulibaly, J. T., Knopp, S., Traoré, M., N'Goran, E. K. and Utzinger, J. (2012). An in-depth analysis of a piece of shit: distribution of Schistosoma mansoni and hookworm eggs in human stool. PLoS Neglected Tropical Diseases 6, e1969.CrossRefGoogle ScholarPubMed
Levecke, B., De Wilde, N., Vandenhoute, E. and Vercruysse, J. (2009). Field validity and feasibility of four techniques for the detection of Trichuris in simians: a model for monitoring drug efficacy in public health? PLoS Neglected Tropical Diseases 3, e366.Google Scholar
Levecke, B., Rinaldi, L., Charlier, J., Maurelli, M. P., Morgoglione, M. E., Vercruysse, J. and Cringoli, G. (2011). Monitoring drug efficacy against gastrointestinal nematodes when faecal egg counts are low: do the analytic sensitivity and the formula matter? Parasitology Research 109, 953957.Google Scholar
Levecke, B., Rinaldi, L., Charlier, J., Maurelli, M. P., Bosco, A., Vercruysse, J. and Cringoli, G. (2012). The precision and accuracy of faecal egg count reduction test results in cattle using McMaster, Cornell-Wisconsin and FLOTAC egg counting methods. Veterinary Parasitology 188, 194199.Google Scholar
McCarthy, J. S., Lustigman, S., Yang, G. J., Barakat, R. M., Garcia, H. H., Sripa, B., Willingham, A. L., Prichard, R. K. and Basáñez, M. G. (2012). A research agenda for helminth diseases of humans: diagnostics for control and elimination programmes. PLoS Neglected Tropical Diseases 6, e1601.Google Scholar
Mekonnen, Z., Meka, S., Ayana, M., Bogers, J., Vercruysse, J. and Levecke, B. (2013). Comparison of individual and pooled stool samples for the assessment of soil-transmitted helminth infection intensity and drug efficacy. PLoS Neglected Tropical Diseases 7, e2189.CrossRefGoogle ScholarPubMed
Montresor, A. (2011). Cure rate is not a valid indicator for assessing drug efficacy and impact of preventive chemotherapy interventions against schistosomiasis and soil-transmitted helminthiasis. Transactions of the Royal Society of Tropical Medicine Hygiene 105, 361363.Google Scholar
Montresor, A., Engels, D., Chitsulo, L., Gabrielli, A., Albonico, M., Savioli, L. and Lammie, P. (2011). The appropriate indicator should be used to assess treatment failure in STH infections. American Journal of Tropical Medicine and Hygiene 85, 579580.Google Scholar
NTD Partner Website (2012). Uniting to Combat Neglected Tropical Diseases. Ending the Neglect and Reaching 2020 Goals. http://www.unitingtocombatntds.org.Google Scholar
Pullan, R. L. and Brooker, S. J. (2012). The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasites and Vectors 5, 81.Google Scholar
Rollinson, D., Knopp, S., Levitz, S., Stothard, J. R., Tchuem Tchuenté, L.-A., Garba, A., Mohammed, K. A., Schur, N., Person, B., Colley, D. G. and Utzinger, J. (2013). Time to set the agenda for schistosomiasis elimination. Acta Tropica 128, 423440.Google Scholar
Sinniah, B. (1982). Daily egg production of Ascaris lumbricoides: the distribution of eggs in the feces and the variability of egg counts. Parasitology 84, 167175.Google Scholar
Sousa-Figueiredo, J. C., Betson, M., Atuhaire, A., Arinaitwe, M., Navaratnam, A. M. D., Kabatereine, N. B., Bickle, Q. and Stothard, J. R. (2012). Performance and safety of praziquantel for treatment of intestinal schistosomiasis in infants and preschool children. PLoS Neglected Tropical Diseases 6, e1864.Google Scholar
Speich, B., Knopp, S., Mohammed, K. A., Khamis, I. S., Rinaldi, L., Cringoli, G., Rollinson, D. and Utzinger, J. (2010). Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys. Parasites and Vectors 3, 71.Google Scholar
Steinmann, P., Utzinger, J., Du, Z. W., Jiang, J. Y., Chen, J. X., Hattendorf, J., Zhou, H. and Zhou, X. N. (2011). Efficacy of single-dose and triple-dose albendazole and mebendazole against soil-transmitted helminths and Taenia spp.: a randomized controlled trial. PLoS One 6, e25003.Google Scholar
Utzinger, J., Rinaldi, L., Lohourignon, L. K., Rohner, F., Zimmermann, M. B., Tschannen, A. B., N'Goran, E. K. and Cringoli, G. (2008). FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 8490.CrossRefGoogle ScholarPubMed
Utzinger, J., N'Goran, E. K., Caffrey, C. R. and Keiser, J. (2011). From innovation to application: social-ecological context, diagnostics, drugs and integrated control of schistosomiasis. Acta Tropica 120 (Suppl.), S121S137.CrossRefGoogle ScholarPubMed
Utzinger, J., Becker, S. L., Knopp, S., Blum, J., Neumayr, A. L., Keiser, J. and Hatz, C. F. (2012). Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Medical Weekly 142, w13727.Google Scholar
Vercruysse, J., Behnke, J. M., Albonico, M., Ame, S. M., Angebault, C., Bethony, J. M., Engels, D., Guillard, B., Nguyen, T. V., Kang, G., Katulla, D., Kotze, A. C., McCarthy, J. S., Mekonnen, Z., Montresor, A., Periago, M. V., Tchuem Tchuenté, L.-A., Dang, T. C., Zeynudin, A. and Levecke, B. (2011). Assessment of the anthelmintic efficacy of albendazole in school children in seven countries where soil-transmitted helminths are endemic. PLoS Neglected Tropical Diseases 5, e948.Google Scholar
Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36, 148.Google Scholar
World Health Organization (1991). Basic Laboratory Methods in Medical Parasitology. World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization (2006). Preventive Chemotherapy in Human Helminthiasis: Coordinated Use of Anthelminthic Drugs in Control Interventions: A Manual for Health Professionals and Programme Managers. World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization (2010). First WHO Report on Neglected Tropical Diseases 2010: Working to Overcome the Global Impact of Neglected Tropical Diseases. World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization (2011). Helminth Control in School-Age Children: A Guide for Managers of Control Programmes, 2nd Edn. World Health Organization, Geneva, Switzerland.Google Scholar
World Health Organization (2013). Assessing the Efficacy of Anthelminthic Drugs against Schistosomiasis and Soil-Transmitted Helminthiasis. World Health Organization, Geneva, Switzerland.Google Scholar
Ye, X. P., Donnelly, C. A., Fu, Y. L. and Wu, Z. X. (1997). The non-randomness of the distribution of Trichuris trichiura and Ascaris lumbricoides in feces and the effect of stirring fecal specimens. Tropical Medicine and International Health 2, 261264.Google Scholar