Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-05-11T19:14:53.329Z Has data issue: false hasContentIssue false

Evaluation of portable microscopic devices for the diagnosis of Schistosoma and soil-transmitted helminth infection

Published online by Cambridge University Press:  24 April 2014

ISAAC I. BOGOCH*
Affiliation:
Divisions of Internal Medicine and Infectious Diseases, Toronto General Hospital, 14EN-209, 200 Elizabeth Street, Toronto, ON, M5G 2C4, Canada
JEAN T. COULIBALY
Affiliation:
Unité de Formation et de Recherche Biosciences, Université Félix Houphouët-Boigny, 22 BP 770, Abidjan 22, Côte d'Ivoire Centre Suisse de Recherches Scientifiques en Côte d'Ivoire, 01 BP 1303, Abidjan 01, Côte d'Ivoire
JASON R. ANDREWS
Affiliation:
Division of Infectious Diseases and Geographic Medicine, Stanford University School of Medicine, Stanford, CA, 94305-5107, USA
BENJAMIN SPEICH
Affiliation:
Department of Medical Parasitology and Infection Biology, Swiss Tropical and Public Health Institute, P.O. Box, CH-4002 Basel, Switzerland University of Basel, P.O. Box, CH-4003 Basel, Switzerland
JENNIFER KEISER
Affiliation:
Department of Medical Parasitology and Infection Biology, Swiss Tropical and Public Health Institute, P.O. Box, CH-4002 Basel, Switzerland University of Basel, P.O. Box, CH-4003 Basel, Switzerland
J. RUSSELL STOTHARD
Affiliation:
Parasitology Department, Liverpool School of Tropical Medicine, Liverpool L3 5QA, UK
ELIÉZER K. N'GORAN
Affiliation:
Unité de Formation et de Recherche Biosciences, Université Félix Houphouët-Boigny, 22 BP 770, Abidjan 22, Côte d'Ivoire Centre Suisse de Recherches Scientifiques en Côte d'Ivoire, 01 BP 1303, Abidjan 01, Côte d'Ivoire
JÜRG UTZINGER
Affiliation:
University of Basel, P.O. Box, CH-4003 Basel, Switzerland Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, P.O. Box, CH-4002 Basel, Switzerland
*
*Corresponding author. Divisions of Internal Medicine and Infectious Diseases, Toronto General Hospital, 14EN-209, 200 Elizabeth Street, Toronto, ON, M5G 2C4, Canada. E-mail: isaac.bogoch@uhn.ca

Summary

The diagnosis of parasitic worm (helminth) infections requires specialized laboratory settings, but most affected individuals reside in locations without access to such facilities. We tested two portable microscopic devices for the diagnosis of helminth infections in a cross-sectional survey in rural Côte d'Ivoire. We examined 164 stool samples under a light microscope and then re-examined with a commercial portable light microscope and an experimental mobile phone microscope for the diagnosis of Schistosoma mansoni and soil-transmitted helminths. Additionally, 180 filtered urine samples were examined by standard microscopy and compared with the portable light microscope for detection of Schistosoma haematobium eggs. Conventional microscopy was considered the diagnostic reference standard. For S. mansoni, S. haematobium and Trichuris trichiura, the portable light microscope showed sensitivities of 84·8%, 78·6% and 81·5%, respectively, and specificities of 85·7%, 91·0% and 93·0%, respectively. For S. mansoni and T. trichiura, we found sensitivities for the mobile phone microscope of 68·2% and 30·8%, respectively, and specificities of 64·3% and 71·0%, respectively. We conclude that the portable light microscope has sufficient diagnostic yield for Schistosoma and T. trichiura infections, while the mobile phone microscope has only modest sensitivity in its current experimental set-up. Development of portable diagnostic technologies that can be used at point-of-sample collection will enhance diagnostic coverage in clinical and epidemiological settings.

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

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.CrossRefGoogle ScholarPubMed
Bogoch, I. I., Andrews, J. R., Dadzie Ephraim, R. K. and Utzinger, J. (2012). Simple questionnaire and urine reagent strips compared to microscopy for the diagnosis of Schistosoma haematobium in a community in northern Ghana. Tropical Medicine and International Health. doi: 10.1111/j.1365-3156.2012.03054.x.CrossRefGoogle Scholar
Bogoch, I. I., Andrews, J. R., Speich, B., Utzinger, J., Ame, S. M., Ali, S. M. and Keiser, J. (2013). Mobile phone microscopy for the diagnosis of soil-transmitted helminth infections: a proof-of-concept study. American Journal of Tropical Medicine and Hygiene 88, 626629.CrossRefGoogle ScholarPubMed
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
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
Coulibaly, J. T., Knopp, S., N'Guessan, N. A., Silué, K. D., Fürst, T., Lohourignon, L. K., Brou, J. K., N'Gbesso, Y. K., Vounatsou, P., N'Goran, E. K. and Utzinger, J. (2011). Accuracy of urine circulating cathodic antigen (CCA) test for Schistosoma mansoni diagnosis in different settings of Côte d'Ivoire. PLoS Neglected Tropical Diseases 5, e1384.Google Scholar
Coulibaly, J. T., Fürst, T., Silué, K. D., Knopp, S., Hauri, D., Ouattara, M., Utzinger, J. and N'Goran, E. K. (2012). Intestinal parasitic infections in schoolchildren in different settings of Côte d'Ivoire: effect of diagnostic approach and implications for control. Parasites & Vectors 5, 135.Google Scholar
Coulibaly, J. T., N'Gbesso, Y. K., N'Guessan, N. A., Winkler, M. S., Utzinger, J. and N'Goran, E. K. (2013). Epidemiology of schistosomiasis in two high-risk communities of south Côte d'Ivoire with particular emphasis on pre-school-aged children. American Journal of Tropical Medicine and Hygiene 89, 3241.CrossRefGoogle ScholarPubMed
de Vlas, S. J. and Gryseels, B. (1992). Underestimation of Schistosoma mansoni prevalences. Parasitology Today 8, 274277.CrossRefGoogle ScholarPubMed
Greenbaum, A., Sikora, U. and Ozcan, A. (2012). Field-portable wide-field microscopy of dense samples using multi-height pixel super-resolution based lensfree imaging. Lab on a Chip 12, 12421245.Google Scholar
Gryseels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. Lancet 368, 11061118.Google Scholar
Gyorkos, T. W., Ramsan, M., Foum, A. and Khamis, I. S. (2001). Efficacy of new low-cost filtration device for recovering Schistosoma haematobium eggs from urine. Journal of Clinical Microbiology 39, 26812682.CrossRefGoogle ScholarPubMed
Hotez, P. J., Brindley, P. J., Bethony, J. M., King, C. H., Pearce, E. J. and Jacobson, J. (2008). Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 13111321.Google Scholar
Isikman, S. O., Greenbaum, A., Lee, M., Bishara, W., Mudanyali, O., Su, T.-W. and Ozcan, A. (2012). Lensfree computational microscopy tools for cell and tissue imaging at the point-of-care and in low-resource settings. Analytical Cellular Pathology (Amsterdam) 35, 229247.CrossRefGoogle ScholarPubMed
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 de São Paulo 14, 397400.Google ScholarPubMed
Keiser, J., N'Goran, E. K., Traoré, M., Lohourignon, K. L., Singer, B. H., Lengeler, C., Tanner, M. and Utzinger, J. (2002). Polyparasitism with Schistosoma mansoni, geohelminths, and intestinal protozoa in rural Côte d'Ivoire. Journal of Parasitology 88, 461466.Google ScholarPubMed
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.Google Scholar
Knopp, S., Becker, S. L., Ingram, K. J., Keiser, J. and Utzinger, J. (2013). Diagnosis and treatment of schistosomiasis in children in the era of intensified control. Expert Review of Anti-Infective Therapy 11, 12371258.Google Scholar
Kongs, A., Marks, G., Verlé, P. and Van der Stuyft, P. (2001). The unreliability of the Kato-Katz technique limits its usefulness for evaluating S. mansoni infections. Tropical Medicine and International Health 6, 163169.Google Scholar
Kosinski, K. C., Bosompem, K. M., Stadecker, M. J., Wagner, A. D., Plummer, J., Durant, J. L. and Gute, D. M. (2011). Diagnostic accuracy of urine filtration and dipstick tests for Schistosoma haematobium infection in a lightly infected population of Ghanaian schoolchildren. Acta Tropica 118, 123127.Google Scholar
Lee, M., Yaglidere, O. and Ozcan, A. (2011). Field-portable reflection and transmission microscopy based on lensless holography. Biomedical Optics Express 2, 27212730.Google Scholar
Linder, E., Grote, A., Varjo, S., Linder, N., Lebbad, M., Lundin, M., Diwan, V., Hannuksela, J. and Lundin, J. (2013). On-chip imaging of Schistosoma haematobium eggs in urine for diagnosis by computer vision. PLoS Neglected Tropical Diseases 7, e2547.Google Scholar
Mott, K. E., Dixon, H., Osei-Tutu, E. and England, E. C. (1983). Relation between intensity of Schistosoma haematobium infection and clinical haematuria and proteinuria. Lancet 1, 10051008.CrossRefGoogle ScholarPubMed
Murray, C. J. L., Vos, T., Lozano, R., Naghavi, M., Flaxman, A. D., Michaud, C. et al. (2012). Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380, 21972223.Google Scholar
Peters, P. A., Mahmoud, A. A., Warren, K. S., Ouma, J. H. and Siongok, T. K. (1976). Field studies of a rapid, accurate means of quantifying Schistosoma haematobium eggs in urine samples. Bulletin of the World Health Organization 54, 159162.Google ScholarPubMed
Robinson, E., Picon, D., Sturrock, H. J., Sabasio, A., Lado, M., Kolaczinski, J. and Brooker, S. (2009). The performance of haematuria reagent strips for the rapid mapping of urinary schistosomiasis: field experience from Southern Sudan. Tropical Medicine and International Health 14, 14841487.CrossRefGoogle ScholarPubMed
Ross, A. G. P., Bartley, P. B., Sleigh, A. C., Olds, G. R., Li, Y., Williams, G. M. and McManus, D. P. (2002). Schistosomiasis. New England Journal of Medicine 346, 12121220.Google Scholar
Smith, Z. J., Chu, K., Espenson, A. R., Rahimzadeh, M., Gryshuk, A., Molinaro, M., Dwyre, D. M., Lane, S., Matthews, D. and Wachsmann-Hogiu, S. (2011). Cell-phone-based platform for biomedical device development and education applications. PLoS One 6, e17150.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 & Vectors 3, 71.CrossRefGoogle ScholarPubMed
Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006). Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infectious Diseases 6, 411425.CrossRefGoogle ScholarPubMed
Steinmann, P., Utzinger, J., Du, Z.-W. and Zhou, X.-N. (2010). Multiparasitism: a neglected reality on global, regional and local scale. Advances in Parasitology 73, 2150.Google Scholar
Stothard, J. R., Kabatereine, N. B., Tukahebwa, E. M., Kazibwe, F., Mathieson, W., Webster, J. P. and Fenwick, A. (2005). Field evaluation of the Meade Readiview handheld microscope for diagnosis of intestinal schistosomiasis in Ugandan school children. American Journal of Tropical Medicine and Hygiene 73, 949955.Google Scholar
Tuijn, C. J., Hoefman, B. J., van Beijma, H., Oskam, L. and Chevrollier, N. (2011). Data and image transfer using mobile phones to strengthen microscopy-based diagnostic services in low and middle income country laboratories. PLoS One 6, e28348.CrossRefGoogle ScholarPubMed
Utzinger, J., Booth, M., N'Goran, E. K., Müller, I., Tanner, M. and Lengeler, C. (2001). Relative contribution of day-to-day and intra-specimen variation in faecal egg counts of Schistosoma mansoni before and after treatment with praziquantel. Parasitology 122, 537544.Google Scholar
WHO (2002). Prevention and control of schistosomiasis and soil-transmitted helminthiasis: a report of a WHO expert committee. WHO Technical Report Series 912, 157.Google Scholar