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Comparison between merthiolate–iodine–formalin and Kato–Katz methods for the diagnosis of human helminth infections in resource-limited settings

Published online by Cambridge University Press:  28 October 2016

R.N. Incani ,
T. Homan ,
E. Pinelli ,
L. Mughini-Gras ,
H. Guevara  and
J. Jesus
R.N. Incani*
Affiliation:
Department of Parasitology, Faculty of Health Sciences, Universidad de Carabobo, Valencia, Venezuela
T. Homan
Affiliation:
Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, The Netherlands
E. Pinelli
Affiliation:
Centre for Infectious Disease Control, National Institute of Public Health and the Environment (RIVM), Bilthoven, The Netherlands
L. Mughini-Gras
Affiliation:
Centre for Infectious Disease Control, National Institute of Public Health and the Environment (RIVM), Bilthoven, The Netherlands Department of Infectious Diseases and Immunology, Utrecht University, Utrecht, the Netherlands
H. Guevara
Affiliation:
Department of Public Health, Faculty of Health Sciences, Universidad de Carabobo, Valencia, Venezuela
J. Jesus
Affiliation:
Department of Parasitology, Faculty of Health Sciences, Universidad de Carabobo, Valencia, Venezuela
*
*E-mail: rincani@uc.edu.ve
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Abstract

Diagnosis of intestinal parasites through examination of fresh faecal samples is hampered by its unpleasantness and the urgent need to detect all parasitic forms. In this paper, we compared the standard Kato–Katz (KK) technique with a traditional fixation method, the merthiolate–iodine–formalin (MIF) method. Two hundred and twenty-seven faecal samples from individuals living in a rural setting in Venezuela with high to moderate prevalences of Ascaris lumbricoides (Al), Trichuris trichiura (Tt) and hookworm infections were examined. The ‘gold standard’ used here was derived from the combination of the outcomes from both methods. KK performed better at detecting Tt, and showed higher sensitivity and negative predictive value for both Tt and Al, probably due to a higher capacity of KK to detect low parasite loads. Both methods showed an almost perfect agreement using the Kappa index. MIF provided a higher median of parasitic loads for low and total egg counts for the three helminths. Differentiating fertile from infertile eggs of Al did not affect the results; infertile eggs were present only at low and intermediate parasitic loads, but absent at high loads. KK was not able to detect high loads of any of the helminths. MIF allowed for the detection of other helminths, such as Strongyloides stercoralis, and protozoan infections, for which KK is not specific. In conclusion, MIF is a simple and inexpensive technique that performs competitively with KK in both laboratory and field work on intestinal helminths, particularly in resource-limited settings.

Type
Research Papers
Information
Journal of Helminthology , Volume 91 , Issue 6 , November 2017 , pp. 657 - 664
Copyright
Copyright © Cambridge University Press 2016 

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References

Ash, L.R. & Orihel, T.C. (1997) Atlas of human parasitology. 4th edn. 410 pp. Chicago, ASCP Press.Google Scholar
Assefa, L.M., Crellen, T., Kepha, S., Kihara, J.H., Njenga, S.M., Pullan, R.L. & Brooker, S.J. (2014) Diagnostic accuracy and cost-effectiveness of alternative methods for detection of soil-transmitted helminths in a post-treatment setting in western Kenya. PLoS Neglected Tropical Diseases 8, e2843. doi:org/10.1371/journal.pntd.0002843.CrossRefGoogle Scholar
Barda, B.D., Rinaldi, L., Ianniello, D., Zepherine, H., Salvo, F., Sadutshang, T., Cringoli, G., Clementi, M. & Albonico, M. (2013) Mini-FLOTAC, an innovative direct diagnostic technique for intestinal parasitic infections: experience from the field. PLoS Neglected Tropical Diseases 6, 220. doi: 101186/1756-3705-6-220.Google Scholar
Barda, B., Cajal, P., Villagran, E., Cimino, R., Juarez, M., Krolewiecki, A. & Rinaldi, L. (2014) Mini-FLOTAC, Kato–Katz and McMaster: three methods, one goal; highlights from north Argentina. Parasites & Vectors 7, 271. doi: 10.1186/1756-3305-7-271.Google Scholar
Barda, B., Cajal, P., Villagran, E., Cimino, R., Juarez, M., Krolewiecki, A., Rinaldi, L., Cringoli, G., Burioni, R., Albonico, M, (2015) How long can stool samples be fixed for an accurate diagnosis of soil-transmitted helminth infection using mini-FLOTAC? PLoS Neglected Tropical Diseases 9, e0003698. doi: 10.1371/journal.pntd.0003698.Google Scholar
Basuni, M., Muhi, J., Othman, N., Verweij, J.J., Ahmad, M., Miswan, N., Rahumatullah, A., Aziz, F.A., Zainudin, N.S. & Noordin, R. (2011) A pentaplex real-time polymerase chain reaction assay for detection of four species of soil-transmitted helminths. American Journal of Tropical Medicine and Hygiene 84, 338–343.Google Scholar
Becker, S.L., Chatigre, J.K., Gohou, J.P., Coulibaly, J.T., Leuppi, R., Polman, K., Chappuis, F., Mertens, P., Herrmann, M., N'Goran, E.K., Utzinger, J. & von Muller, L. (2015) Combined stool-based multiplex PCR and microscopy for enhanced pathogen detection in patients with persistent diarrhoea and asymptomatic controls from Cote d'Ivoire. Clinical Microbiology and Infection 21, 591.el–591.e10.Google Scholar
Cringoli, G., Rinaldi, L., Maurelli, M.P. & Utzinger, J. (2010) FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nature Protocols 5, 503–515.Google Scholar
Dacombe, R.J., Crampin, A.C., Floyd, S., Randall, A., Ndhlovu, R., Bickle, Q. & Fine, P.E.M. (2007) Time delays between patient and laboratory selectively affect accuracy of helminth diagnosis. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 140–145.Google Scholar
Dunn, J.C., Turner, H.C., Tun, A. & Anderson, R.M. (2016) Epidemiological surveys of, and research on, soil-transmitted helminths in Southeast Asia: a systematic review. Parasites & Vectors 9, 31. doi: 10.1186/s13071-016-1310-2.Google Scholar
Glinz, D., Silue, K.D., Knopp, S., Lohourignon, L.K., Yao, K.P., Steinmann, P., Rinaldi, L., Cringoli, G., N'Goran, E.K. & 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. doi: 10.3771/journal.pntd.0000754.Google Scholar
Goodman, D., Haji, H.J., Bickle, Q.D., Stoltzfus, R.J., Tielsch, J.M., Ramsan, M., Savioli, L. & Albonico, M. (2007) A comparison of methods for detecting the eggs of Ascaris, Trichuris, and hookworm in infant stool, and the epidemiology of infection in Zanzibari infants. American Journal of Tropical Medicine and Hygiene 76, 725–731.Google Scholar
Homan, T. (2009) Identifying risk factors and the reacquisition of infection with Ascaris lumbricoides in a rural community, central north Venezuela. MSc thesis, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam.Google Scholar
Hotez, P.J., Bundy, D.A.P., Beegle, K., Brooker, S., Drake, L., de Silva, N., Montresor, A., Engels, D., Jukes, M., Chitsulo, L., Chow, J., Laxminarayan, R., Michaud, C., Bethony, J., Correa-Oliveira, R., Shuhua, X., Fenwick, A. & Savioli, L. (2006) Helminth infections: soil-transmitted helminth infections and schistosomiasis. pp. 467–482 in Jamison, D.T., Breman, J.G., Measham, A.R., Alleyne, G., Claeson, M., Evans, D.B., Jha, P., Mills, A. & Musgrove, P. (Eds) Disease control priorities in developing countries. 2nd edn. Washington, DC, World Bank.Google Scholar
Hotez, P.J., Brindley, P.J., Bethony, J.M., King, C.H., Pearce, E.J. & Jacobson, J. (2008) Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 1311–1321.Google Scholar
Katz, N., Chaves, A. & Pellegrino, J. (1972) A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Revista do Instituto de Medicina Topical de São Paulo 14, 397–400.Google Scholar
Knopp, S., Mgeni, A.F., Khamis, I.S., Steinmann, P., Stothard, J.R., Rollinson, D., Marti, H. & 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. doi: 10.1371/journal.pntd.0000331.CrossRefGoogle ScholarPubMed
Knopp, S., Speich, B., Hattendorf, J., Rinaldi, L., Mohammed, K.A., Khamis, I.S., Mohammed, A.S., Albonico, M., Rollinson, D., Marti, H., Cringoli, G. & Utzinger, J. (2011) Diagnostic accuracy of Kato–Katz and FLOTAC for assessing anthelmintic drug efficacy. PLoS Neglected Tropical Diseases 5, e1036. doi: 10.1371/journal.pntd.0001036.Google Scholar
Levecke, B., Behnke, J.M., Ajjampur, S.S., Albonico, M., Ame, S.M., Charlier, J., Geiger, S.M., Hoa, N.T., Kamwa Ngassam, R.I., Kotze, A.C., McCarthy, J.S., Montresor, A., Periago, M.V., Roy, S., Tchuem Tchuente, L.A., Thach, D.T. & Vercruysse, J. (2011) A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato–Katz thick smear methods for soil-transmitted helminths. PLoS Neglected Tropical Diseases 5, e1201. doi: 10.1371/journal.pntd.0001201.Google Scholar
Mank, T.G., Zaat, J.O., Blotkamp, J. & Polderman, A.M. (1995) Comparison of fresh versus sodium acetate acetic acid formalin preserved stool specimens for diagnosis of intestinal protozoal infections. European Journal of Clinical Microbiology and Infectious Diseases 14, 1076–1081.Google Scholar
Montresor, A., Cromptom, D.W.T., Hall, H., Bundy, D.A.P. & Savioli, L. (1998) Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at community level. A guide for control programme managers. WHO/CTD/SIP98.1. Geneva, World Health Organization.Google Scholar
Nikolay, B., Brooker, S.J. & Pullan, R.L. (2014) Sensitivity of diagnostic tests for human soil-transmitted helminth infections: a meta-analysis in the absence of a true gold standard. International Journal of Parasitology 44, 765–774.Google Scholar
Periago, M.V., Diniz, R.C., Pinto, S.A., Yakovleva, A., Correa-Oliveira, R., Diemert, D.J. & Bethony, J.M. (2015) The right tool for the job: detection of soil-transmitted helminths in areas co-endemic for other helminths. PLoS Neglected Tropical Diseases 9, e0003967. doi:10.1371/journal.pntd.0003967.Google Scholar
Pietrzak-Johnston, S.M., Bishop, H., Wahlquist, S., Moura, H., Da Silva, N.D., Da Silva, S.P. & Nguyen-Dinh, P. (2000) Evaluation of commercially available preservatives for laboratory detection of helminths and protozoa in human fecal specimens. Journal of Clinical Microbiology 38, 1959–1964.Google Scholar
Pullan, R.L., Smith, J.L., Jasrasaria, R. & Brooker, S.J. (2014) Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasites & Vectors 7, 37. doi: 10.1186/1756-3305-7-37.Google Scholar
Sapero, J.J. & Lawless, D.K. (1953) The MIF stain-preservation technic for the identification of intestinal protozoa. American Journal of Tropical Medicine and Hygiene 2, 613–619.Google Scholar
Steinmann, P., Du, Z.W., Wang, L.B., Wang, X.Z., Jiang, J.Y., Li, L.H., Marti, H., Zhou, X.N. & Utzinger, J. (2008) Extensive multiparasitism in a village of Yunnan province, People's Republic of China, revealed by a suite of diagnostic methods. American Journal of Tropical Medicine and Hygiene 78, 760–769.Google Scholar
Stoltzfus, R.J., Chwaya, H.M., Tielsch, J.M., Schulze, K.J., Albonico, M. & Savioli, L. (1997) Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms. American Journal of Clinical Nutrition 65, 153–159.Google Scholar
Tarafder, M.R., Carabin, H., Joseph, L., Balolong, E. Jr, Olveda, R. & McGarvey, S.T. (2010) Estimating the sensitivity and specificity of Kato–Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a ‘gold standard’. International Journal of Parasitology 40, 399–404.Google Scholar
Utzinger, J., Rinaldi, L., Lohourignon, L.K., Rohner, F., Zimmermann, M.B., Tschannen, A.B., N'Goran, E.K. & 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, 84–90.Google Scholar
Vandenberg, O., Van Laethem, Y., Souayah, H., Kutane, W.T., van Gool, T. & Dediste, A. (2006) Improvement of routine diagnosis of intestinal parasites with multiple sampling and SAF-fixative in the triple-faeces-test. Acta Gastro-Enterologica Belgica 69, 361–366.Google Scholar
Verweij, J.J. & van Lieshout, L. (2011) Intestinal parasitic infections in an industrialized country; a new focus on children with better DNA-based diagnostics. Parasitology 138, 1492–1498.Google Scholar
WHO (1991) Basic laboratory methods in medical parasitology. pp. 25–28. Geneva, World Health Organization.Google Scholar
WHO (2002) Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Report of a WHO Expert Committee, WHO Technical Report Series 912. Geneva, World Health Organization.Google Scholar