New diagnostic tools in schistosomiasis

Clinical Microbiology and Infection

Volumn 21, Issue 6, 2015, Pages 529-542

  Utzinger, J ^a,b   Becker, S L ^a,b,c   van Lieshout, L ^d   van Dam, G J ^d   Knopp, S ^a,b,e  

^a SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c SAARLAND UNIVERSITY   (Germany)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

Antibody detection; Circulating antigens; Control; Diagnosis; Elimination; Kato Katz; Polymerase chain reaction; Schistosoma; Serology; Urine filtration

Indexed keywords

ANTIGEN DETECTION; CLINICAL PRACTICE; FECES ANALYSIS; HUMAN; MEDICAL ASSESSMENT; MICROSCOPY; MORBIDITY; NONHUMAN; PATIENT CARE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; SCHISTOSOMIASIS; SEROLOGY; URINALYSIS; WORLD HEALTH ORGANIZATION; DIAGNOSTIC TEST; DISEASE ERADICATION; DRUG MONITORING; IMMUNOASSAY; LABORATORY TEST; PROCEDURES;

SCHISTOSOMA;

BIOLOGICAL MARKER;

BIOMARKERS; CLINICAL LABORATORY TECHNIQUES; DIAGNOSTIC TESTS, ROUTINE; DISEASE ERADICATION; DRUG MONITORING; HUMANS; IMMUNOASSAY; MICROSCOPY; POLYMERASE CHAIN REACTION; SCHISTOSOMIASIS;

EID: 84930819439     PISSN: 1198743X     EISSN: 14690691     Source Type: Journal    
DOI: 10.1016/j.cmi.2015.03.014     Document Type: Review

References (125)

1. Steinmann P., Keiser J., Bos R., Tanner M., Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 2006, 6:411-425.
2. Gryseels B., Polman K., Clerinx J., Kestens L. Human schistosomiasis. Lancet 2006, 368:1106-1118.
3. Colley D.G., Bustinduy A.L., Secor W.E., King C.H. Human schistosomiasis. Lancet 2014, 383:2253-2264.
4. Huang Y.X., Manderson L. The social and economic context and determinants of schistosomiasis japonica. Acta Trop 2005, 96:223-231.
5. Utzinger J., N'Goran E.K., Caffrey C.R., Keiser J. From innovation to application: social-ecological context, diagnostics, drugs and integrated control of schistosomiasis. Acta Trop 2011, 120(Suppl.1):S121-S137.
6. Grimes J.E.T., Croll D., Harrison W.E., Utzinger J., Freeman M.C., Templeton M.R. The relationship between water, sanitation and schistosomiasis: a systematic review and meta-analysis. PLoS Negl Trop Dis 2014, 8:e3296.
7. Gryseels B. Schistosomiasis. Infect Dis Clin North Am 2012, 26:383-397.
8. Murray C.J.L., Vos T., Lozano R., Naghavi M., Flaxman A.D., Michaud C., et al. 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 2012, 380:2197-2223.
9. Hotez P.J., Alvarado M., Basáñez M.G., Bolliger I., Bourne R., Boussinesq M., et al. The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl Trop Dis 2014, 8:e2865.
10. Martens W.J.M., Jetten T.H., Rotmans J., Niessen L.W. Climate change and vector-borne diseases: a global modeling perspective. Glob Environ Change 1995, 5:195-209.
11. Martens W.J.M., Jetten T.H., Focks D.A. Sensitivity of malaria, schistosomiasis and dengue to global warming. Climatic Change 1997, 35:145-156.
12. Zhou X.N., Yang G.J., Yang K., Wang X.H., Hong Q.B., Sun L.P., et al. Potential impact of climate change on schistosomiasis transmission in China. Am J Trop Med Hyg 2008, 78:188-194.
13. Abou-El-Naga I.F. Biomphalaria alexandrina in Egypt: past, present and future. JBiosci 2013, 38:665-672.
14. McCreesh N., Booth M. Challenges in predicting the effects of climate change on Schistosoma mansoni and Schistosoma haematobium transmission potential. Trends Parasitol 2013, 29:548-555.
15. Pedersen U.B., Midzi N., Mduluza T., Soko W., Stensgaard A.S., Vennervald B.J., et al. Modelling spatial distribution of snails transmitting parasitic worms with importance to human and animal health and analysis of distributional changes in relation to climate. Geospat Health 2014, 8:335-343.
16. Rollinson D., Knopp S., Levitz S., Stothard J.R., Tchuem Tchuenté L.A., Garba A., et al. Time to set the agenda for schistosomiasis elimination. Acta Trop 2013, 128:423-440.
17. Berry A., Moné H., Iriart X., Mouahid G., Aboo O., Boissier J., et al. Schistosomiasis haematobium, Corsica, France. Emerg Infect Dis 2014, 20:1595-1597.
18. Holtfreter M.C., Moné H., Müller-Stöver I., Mouahid G., Richter J. Schistosoma haematobium infections acquired in Corsica, France, August 2013. Euro Surveill 2014, 19.
19. Clerinx J., van Gompel A. Schistosomiasis in travellers and migrants. Travel Med Infect Dis 2011, 9:6-24.
20. WHO Preventive chemotherapy in human helminthiasis: coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers 2006, 1-74. World Health Organization, Geneva.
21. WHO Schistosomiasis: progress report 2001-2011 and strategic plan 2012-2020 2013, 1-80. World Health Organization, Geneva.
22. Knopp S., Mohammed K.A., Ali S.M., Khamis I.S., Ame S.M., Albonico M., et al. Study and implementation of urogenital schistosomiasis elimination in Zanzibar (Unguja and Pemba islands) using an integrated multidisciplinary approach. BMC Public Health 2012, 12:930.
23. Utzinger J., Raso G., Brooker S., de Savigny D., Tanner M., Ørnbjerg N., et al. Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution. Parasitology 2009, 136:1859-1874.
24. Bergquist R., Yang G.J., Knopp S., Utzinger J., Tanner M. Surveillance and response: tools and approaches for the elimination stage of neglected tropical diseases. Acta Trop 2015, 141:229-234.
25. Bergquist R., Johansen M.V., Utzinger J. Diagnostic dilemmas in helminthology: what tools to use and when?. Trends Parasitol 2009, 25:151-156.
26. Solomon A.W., Engels D., Bailey R.L., Blake I.M., Brooker S., Chen J.X., et al. Adiagnostics platform for the integrated mapping, monitoring, and surveillance of neglected tropical diseases: rationale and target product profiles. PLoS Negl Trop Dis 2012, 6:e1746.
27. WHO Research priorities for helminth infections. Technical Report of the TDR Disease Reference Group on Helminth Infections 2012, 1-196. World Health Organization, Geneva.
28. Knopp S., Becker S.L., Ingram K., Keiser J., Utzinger J. Diagnosis and treatment of schistosomiasis in children in the era of intensified control. Expert Rev Anti Infect Ther 2013, 11:1237-1258.
29. Stothard J.R., Stanton M.C., Bustinduy A.L., Sousa-Figueiredo J.C., van Dam G.J., Betson M., et al. Diagnostics for schistosomiasis in Africa and Arabia: a review of present options in control and future needs for elimination. Parasitology 2014, 141:1947-1961.
30. Montresor A., Crompton D.W.T., Hall A., Bundy D.A.P., Savioli L. Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at community level 1998, 1-49. World Health Organization, Geneva.
31. Trouiller P., Olliaro P., Torreele E., Orbinski J., Laing R., Ford N. Drug development for neglected diseases: a deficient market and a public-health policy failure. Lancet 2002, 359:2188-2194.
32. Pedrique B., Strub-Wourgaft N., Some C., Olliaro P., Trouiller P., Ford N., et al. The drug and vaccine landscape for neglected diseases (2000-11): a systematic assessment. Lancet Glob Health 2013, 1:e371-e379.
33. Keiser J., Utzinger J. Advances in the discovery and development of trematocidal drugs. Expert Opin Drug Discov 2007, 2:S9-23.
34. WHO Prevention and control of schistosomiasis and soil-transmitted helminthiasis: report of a WHO expert committee. WHO Tech Rep Ser 2002, 912:1-57.
35. Engels D., Chitsulo L., Montresor A., Savioli L. The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Trop 2002, 82:139-146.
36. WHO Accelerating work to overcome the global impact of neglected tropical diseases - a roadmap for implementation 2012, 1-42. World Health Organization, Geneva.
37. th World Health Assembly, Geneva, 21-26 May 2012: Resolutions, decisions and annexes 2012, 36-37. World Health Organization, Geneva.
38. Bossuyt P.M., Reitsma J.B., Bruns D.E., Gatsonis C.A., Glasziou P.P., Irwig L.M., et al. Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative. BMJ 2003, 326:41-44.
39. Simel D.L., Rennie D., Bossuyt P.M. The STARD statement for reporting diagnostic accuracy studies: application to the history and physical examination. JGen Intern Med 2008, 23:768-774.
40. Glinz D., Silué K.D., Knopp S., Lohourignon L.K., Yao K.P., Steinmann P., et al. Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Negl Trop Dis 2010, 4:e754.
41. van Dam G.J., Xu J., Bergquist R., de Dood C.J., Utzinger J., Qin Z.Q., et al. An ultra-sensitive assay targeting the circulating anodic antigen for the diagnosis of Schistosoma japonicum in a low-endemic area, People's Republic of China. Acta Trop 2015, 141:190-197.
42. Knopp S., Corstjens PLAM, Koukounari A., Cercamondi C.I., Ame S.M., de Dood C.J., et al. Sensitivity and specificity of a urine circulating anodic antigen test for the diagnosis of Schistosoma haematobium in low endemic settings. PLoS Negl Trop Dis 2015, 9:e0003752.
43. Colley D.G., Binder S., Campbell C., King C.H., Tchuem Tchuenté L.A., N'Goran E.K., et al. Afive-country evaluation of a point-of-care circulating cathodic antigen urine assay for the prevalence of Schistosoma mansoni. Am J Trop Med Hyg 2013, 88:426-432.
44. King C.H., Bertsch D. Meta-analysis of urine heme dipstick diagnosis of Schistosoma haematobium infection, including low-prevalence and previously-treated populations. PLoS Negl Trop Dis 2013, 7:e2431.
45. The Red Urine Study Group Identification of high-risk communities for schistosomiasis in Africa: a multicountry study. SER Project Reports 1995, 1-103. World Health Organization, Geneva.
46. Lengeler C., Utzinger J., Tanner M. Questionnaires for rapid screening of schistosomiasis in sub-Saharan Africa. Bull World Health Organ 2002, 80:235-242.
47. Bassiouny H.K., Hasab A.A., El-Nimr N.A., Al-Shibani L.A., Al-Waleedi A.A. Rapid diagnosis of schistosomiasis in Yemen using a simple questionnaire and urine reagent strips. East Mediterr Health J 2014, 20:242-249.
48. Emukah E., Gutman J., Eguagie J., Miri E.S., Yinkore P., Okocha N., et al. Urine heme dipsticks are useful in monitoring the impact of praziquantel treatment on Schistosoma haematobium in sentinel communities of Delta state, Nigeria. Acta Trop 2012, 122:126-131.
49. Knopp S., Person B., Ame S.M., Mohammed K.A., Ali S.M., Khamis I.S., et al. Elimination of schistosomiasis transmission in Zanzibar: baseline findings before the onset of a randomized intervention trial. PLoS Negl Trop Dis 2013, 7:e2474.
50. Stothard J.R., Sousa-Figueiredo J.C., Betson M., Adriko M., Arinaitwe M., Rowell C., et al. Schistosoma mansoni infections in young children: when are schistosome antigens in urine, eggs in stool and antibodies to eggs first detectable?. PLoS Negl Trop Dis 2011, 5:e938.
51. Coulibaly J.T., Knopp S., N'Guessan N.A., Silué K.D., Fürst T., Lohourignon L.K., et al. Accuracy of urine circulating cathodic antigen (CCA) test for Schistosoma mansoni diagnosis in different settings of Côte d'Ivoire. PLoS Negl Trop Dis 2011, 5:e1384.
52. Shane H.L., Verani J.R., Abudho B., Montgomery S.P., Blackstock A.J., Mwinzi P.N., et al. Evaluation of urine CCA assays for detection of Schistosoma mansoni infection in Western Kenya. PLoS Negl Trop Dis 2011, 5:e951.
53. Tchuem Tchuenté L.A., Kuete Fouodo C.J., Kamwa Ngassam R.I., Dongmo Noumedem C., Kenfack C.M., Gipwe N.F., et al. Evaluation of circulating cathodic antigen (CCA) urine-tests for diagnosis of Schistosoma mansoni infection in Cameroon. PLoS Negl Trop Dis 2012, 6:e1758.
54. Coulibaly J.T., N'Gbesso Y.K., Knopp S., N'Guessan N.A., Silué K.D., van Dam G.J., et al. Accuracy of urine circulating cathodic antigen test for the diagnosis of Schistosoma mansoni in preschool-aged children before and after treatment. PLoS Negl Trop Dis 2013, 7:e2109.
55. Mwinzi P.N.M., Kittur N., Ochola E., Cooper P.J., Campbell C.H., King C.H., et al. Additional evaluation of the point-of-contact circulating cathodic antigen assay for Schistosoma mansoni infection. Frontiers Public Health 2015, 3.
56. van Dam G.J., Odermatt P., Acosta L., Bergquist R., de Dood C.J., Kornelis D., et al. Evaluation of banked urine samples for the detection of circulating anodic and cathodic antigens in Schistosoma mekongi and S.japonicum infections: a proof-of-concept study. Acta Trop 2015, 141:198-203.
57. Adriko M., Standley C.J., Tinkitina B., Tukahebwa E.M., Fenwick A., Fleming F.M., et al. Evaluation of circulating cathodic antigen (CCA) urine-cassette assay as a survey tool for Schistosoma mansoni in different transmission settings within Bugiri district, Uganda. Acta Trop 2014, 136:50-57.
58. Lamberton P.H., Kabatereine N.B., Oguttu D.W., Fenwick A., Webster J.P. Sensitivity and specificity of multiple Kato-Katz thick smears and a circulating cathodic antigen test for Schistosoma mansoni diagnosis pre- and post-repeated-praziquantel treatment. PLoS Negl Trop Dis 2014, 8:e3139.
59. Peters P.A., Mahmoud A.A., Warren K.S., Ouma J.H., Siongok T.K. Field studies of a rapid, accurate means of quantifying Schistosoma haematobium eggs in urine samples. Bull World Health Organ 1976, 54:159-162.
60. Braun-Munzinger R.A., Southgate B.A. Repeatability and reproducibility of egg counts of Schistosoma haematobium in urine. Trop Med Parasitol 1992, 43:149-154.
61. van Lieshout L., Polderman A.M., Deelder A.M. Immunodiagnosis of schistosomiasis by determination of the circulating antigens CAA and CCA, in particular in individuals with recent or light infections. Acta Trop 2000, 77:69-80.
62. Vinkeles Melchers N.V., van Dam G.J., Shaproski D., Kahama A.I., Brienen E.A., Vennervald B.J., et al. Diagnostic performance of Schistosoma real-time PCR in urine samples from Kenyan children infected with Schistosoma haematobium: day-to-day variation and follow-up after praziquantel treatment. PLoS Negl Trop Dis 2014, 8:e2807.
63. Ephraim R.K., Duah E., Andrews J.R., Bogoch II. Ultra-low-cost urine filtration for Schistosoma haematobium diagnosis: a proof-of-concept study. Am J Trop Med Hyg 2014, 91:544-546.
64. WHO Basic laboratory methods in medical parasitology 1991, 1-69. World Health Organization, Geneva.
65. WHO Bench aids for the diagnosis of intestinal parasites 1994, 1-20. World Health Organization, Geneva.
66. Barda B.D., Rinaldi L., Ianniello D., Zepherine H., Salvo F., Sadutshang T., et al. Mini-FLOTAC, an innovative direct diagnostic technique for intestinal parasitic infections: experience from the field. PLoS Negl Trop Dis 2013, 7:e2344.
67. Utzinger J., Botero-Kleiven S., Castelli F., Chiodini P.L., Edwards H., Köhler N., et al. Microscopic diagnosis of sodium acetate-acetic acid-formalin-fixed stool samples for helminths and intestinal protozoa: a comparison among European reference laboratories. Clin Microbiol Infect 2010, 16:267-273.
68. Katz N., Chaves A., Pellegrino J. Asimple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop São Paulo 1972, 14:397-400.
69. Yap P., Fürst T., Müller I., Kriemler S., Utzinger J., Steinmann P. Determining soil-transmitted helminth infection status and physical fitness of school-aged children. JVis Exp 2012, e3966.
70. Utzinger J., Booth M., N'Goran E.K., Müller I., Tanner M., Lengeler C. Relative contribution of day-to-day and intra-specimen variation in faecal egg counts of Schistosoma mansoni before and after treatment with praziquantel. Parasitology 2001, 122:537-544.
71. Koukounari A., Donnelly C.A., Moustaki I., Tukahebwa E.M., Kabatereine N.B., Wilson S., et al. Alatent Markov modelling approach to the evaluation of circulating cathodic antigen strips for schistosomiasis diagnosis pre- and post-praziquantel treatment in Uganda. PLoS Comput Biol 2013, 9:e1003402.
72. Bogoch I.I., Coulibaly J.T., Andrews J.R., Speich B., Keiser J., Stothard J.R., et al. Evaluation of portable microscopic devices for the diagnosis of Schistosoma and soil-transmitted helminth infection. Parasitology 2014, 141:1811-1818.
73. Cringoli G. FLOTAC, a novel apparatus for a multivalent faecal egg count technique. Parassitologia 2006, 48:381-384.
74. Utzinger J., Rinaldi L., Lohourignon L.K., Rohner F., Zimmermann M.B., Tschannen A.B., et al. FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Trans R Soc Trop Med Hyg 2008, 102:84-90.
75. Knopp S., Glinz D., Rinaldi L., Mohammed K.A., N'Goran E.K., Stothard J.R., et al. FLOTAC: a promising technique for detecting helminth eggs in human faeces. Trans R Soc Trop Med Hyg 2009, 103:1190-1194.
76. Cringoli G., Rinaldi L., Maurelli M.P., Utzinger J. FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc 2010, 5:503-515.
77. Cringoli G., Rinaldi L., Albonico M., Bergquist R., Utzinger J. Geospatial (s)tools: integration of advanced epidemiological sampling and novel diagnostics. Geospat Health 2013, 7:399-404.
78. Barda B., Albonico M., Ianniello D., Ame S.M., Keiser J., Speich B., et al. How long can stool samples be fixed for an accurate diagnosis of soil-transmitted helminth infection using Mini-FLOTAC?. PLoS Negl Trop Dis 2015, 9:e0003698.
79. Barda B., Zepherine H., Rinaldi L., Cringoli G., Burioni R., Clementi M., et al. Mini-FLOTAC and Kato-Katz: helminth eggs watching on the shore of Lake Victoria. Parasit Vectors 2013, 6:220.
80. Nausch N., Dawson E.M., Midzi N., Mduluza T., Mutapi F., Doenhoff M.J. Field evaluation of a new antibody-based diagnostic for Schistosoma haematobium and S.mansoni at the point-of-care in northeast Zimbabwe. BMC Infect Dis 2014, 14:165.
81. Poole H., Terlouw D.J., Naunje A., Mzembe K., Stanton M., Betson M., et al. Schistosomiasis in pre-school-age children and their mothers in Chikhwawa district, Malawi with notes on characterization of schistosomes and snails. Parasit Vectors 2014, 7:153.
82. Bierman W.F., Wetsteyn J.C., van Gool T. Presentation and diagnosis of imported schistosomiasis: relevance of eosinophilia, microscopy for ova, and serology. JTravel Med 2005, 12:9-13.
83. Meltzer E., Schwartz E. Schistosomiasis: current epidemiology and management in travelers. Curr Infect Dis Rep 2013, 15:211-215.
84. van Gool T., Vetter H., Vervoort T., Doenhoff M.J., Wetsteyn J., Overbosch D. Serodiagnosis of imported schistosomiasis by a combination of a commercial indirect hemagglutination test with Schistosoma mansoni adult worm antigens and an enzyme-linked immunosorbent assay with S.mansoni egg antigens. JClin Microbiol 2002, 40:3432-3437.
85. Deutsche Gesellschaft für Tropenmedizin und Internationale Gesundheit (DTG): S1-Leitlinie: Diagnostik und Therapie der Schistosomiasis (Bilharziose). Version 07/2013 [in German]. Electronically published: [accessed 21.03.2015]. http://www.dtg.org/uploads/media/Leitlinie_Schistosomiasis.pdf.
86. Nickel B., Sayasone S., Vonghachack Y., Odermatt P., Marti H. Schistosoma mansoni antigen detects Schistosoma mekongi infection. Acta Trop 2015, 141:310-314.
87. Smith H., Doenhoff M., Aitken C., Bailey W., Ji M., Dawson E., et al. Comparison of Schistosoma mansoni soluble cercarial antigens and soluble egg antigens for serodiagnosing schistosome infections. PLoS Negl Trop Dis 2012, 6:e1815.
88. Coulibaly J.T., N'Goran E.K., Utzinger J., Doenhoff M.J., Dawson E.M. Anew rapid diagnostic test for detection of anti-Schistosoma mansoni and anti-Schistosoma haematobium antibodies. Parasit Vectors 2013, 6:29.
89. Dawson E., Sousa-Figueiredo J.C., Kabatereine N., Doenhoff M., Stothard J.R. Intestinal schistosomiasis in pre school-aged children of Lake Albert, Uganda: diagnostic accuracy of a rapid test for detection of anti-schistosome antibodies. Trans R Soc Trop Med Hyg 2013, 107:639-647.
90. Corstjens P.L.A.M., van Lieshout L., Zuiderwijk M., Kornelis D., Tanke H.J., Deelder A.M., et al. Up-converting phosphor technology-based lateral flow assay for detection of Schistosoma circulating anodic antigen in serum. JClin Microbiol 2008, 46:171-176.
91. van Dam G.J., de Dood C.J., Lewis M., Deelder A.M., van Lieshout L., Tanke H.J., et al. Arobust dry reagent lateral flow assay for diagnosis of active schistosomiasis by detection of Schistosoma circulating anodic antigen. Exp Parasitol 2013, 135:274-282.
92. Corstjens P.L.A.M., de Dood C.J., Kornelis D., Fat E.M., Wilson R.A., Kariuki T.M., et al. Tools for diagnosis, monitoring and screening of Schistosoma infections utilizing lateral-flow based assays and upconverting phosphor labels. Parasitology 2014, 141:1841-1855.
93. de Jonge N., Fillié Y.E., Hilberath G.W., Krijger F.W., Lengeler C., de Savigny D.H., et al. Presence of the schistosome circulating anodicantigen (CAA) in urine of patients with Schistosoma mansoni or S.haematobium infections. Am J Trop Med Hyg 1989, 41:563-569.
94. van Dam G.J., Bogitsh B.J., van Zeyl R.J., Rotmans J.P., Deelder A.M. Schistosoma mansoni: invitro and invivo excretion of CAA and CCA by developing schistosomula and adult worms. JParasitol 1996, 82:557-564.
95. Verweij J.J., Stensvold C.R. Molecular testing for clinical diagnosis and epidemiological investigations of intestinal parasitic infections. Clin Microbiol Rev 2014, 27:371-418.
96. Aryeetey Y.A., Essien-Baidoo S., Larbi I.A., Ahmed K., Amoah A.S., Obeng B.B., et al. Molecular diagnosis of Schistosoma infections in urine samples of school children in Ghana. Am J Trop Med Hyg 2013, 88:1028-1031.
97. Pillay P., Taylor M., Zulu S.G., Gundersen S.G., Verweij J.J., Hoekstra P., et al. Real-time polymerase chain reaction for detection of Schistosoma DNA in small-volume urine samples reflects focal distribution of urogenital schistosomiasis in primary school girls in KwaZulu Natal, South Africa. Am J Trop Med Hyg 2014, 90:546-552.
98. Schwarz N.G., Rakotozandrindrainy R., Heriniaina J.N., Randriamampionona N., Hahn A., Hogan B., et al. Schistosoma mansoni in schoolchildren in a Madagascan highland school assessed by PCR and sedimentation microscopy and Bayesian estimation of sensitivities and specificities. Acta Trop 2014, 134:89-94.
99. Kenguele H.M., Adegnika A.A., Nkoma A.M., Ateba-Ngoa U., Mbong M., Zinsou J., et al. Impact of short-time urine freezing on the sensitivity of an established Schistosoma real-time PCR assay. Am J Trop Med Hyg 2014, 90:1153-1155.
100. Lodh N., Naples J.M., Bosompem K.M., Quartey J., Shiff C.J. Detection ofparasite-specific DNA in urine sediment obtained by filtration differentiates between single and mixed infections of Schistosoma mansoni and S.haematobium from endemic areas in Ghana. PLoS One 2014, 9:e91144.
101. Kjetland E.F., Hove R.J., Gomo E., Midzi N., Gwanzura L., Mason P., et al. Schistosomiasis PCR in vaginal lavage as an indicator of genital Schistosoma haematobium infection in rural Zimbabwean women. Am J Trop Med Hyg 2009, 81:1050-1055.
102. Downs J.A., van Dam G.J., Changalucha J.M., Corstjens P.L.A.M., Peck R.N., de Dood C.J., et al. Association of schistosomiasis and HIV infection in Tanzania. Am J Trop Med Hyg 2012, 87:868-873.
103. Huyse T., Webster B.L., Geldof S., Stothard J.R., Diaw O.T., Polman K., et al. Bidirectional introgressive hybridization between a cattle and human schistosome species. PLoS Pathog 2009, 5:e1000571.
104. Webster B.L., Diaw O.T., Seye M.M., Webster J.P., Rollinson D. Introgressive hybridization of Schistosoma haematobium group species in Senegal: species barrier break down between ruminant and human schistosomes. PLoS Negl Trop Dis 2013, 7:e2110.
105. Wichmann D., Panning M., Quack T., Kramme S., Burchard G.D., Grevelding C., et al. Diagnosing schistosomiasis by detection of cell-free parasite DNA in human plasma. PLoS Negl Trop Dis 2009, 3:e422.
106. Kato-Hayashi N., Yasuda M., Yuasa J., Isaka S., Haruki K., Ohmae H., et al. Use of cell-free circulating schistosome DNA in serum, urine, semen, and saliva to monitor a case of refractory imported schistosomiasis hematobia. JClin Microbiol 2013, 51:3435-3438.
107. Cnops L., Soentjens P., Clerinx J., Van Esbroeck M. ASchistosoma haematobium-specific real-time PCR for diagnosis of urogenital schistosomiasis in serum samples of international travelers and migrants. PLoS Negl Trop Dis 2013, 7:e2413.
108. van Lieshout L., Roestenberg M. Clinical consequences of new diagnostic tools for intestinal parasites. Clin Microbiol Infect 2015, [in this issue].
109. Fernández-Soto P., Gandasegui Arahuetes J., Sánchez Hernández A., López Abán J., Vicente Santiago B., Muro A. Aloop-mediated isothermal amplification (LAMP) assay for early detection of Schistosoma mansoni in stool samples: a diagnostic approach in a murine model. PLoS Negl Trop Dis 2014, 8:e3126.
110. Bustinduy A.L., Sousa-Figueiredo J.C., Adriko M., Betson M., Fenwick A., Kabatereine N., et al. Fecal occult blood and fecal calprotectin as point-of-care markers of intestinal morbidity in Ugandan children with Schistosoma mansoni infection. PLoS Negl Trop Dis 2013, 7:e2542.
111. Hatz C.F. The use of ultrasound in schistosomiasis. Adv Parasitol 2001, 48:225-284.
112. Becker S.L., Vogt J., Knopp S., Panning M., Warhurst D.C., Polman K., et al. Persistent digestive disorders in the tropics: causative infectious pathogens and reference diagnostic tests. BMC Infect Dis 2013, 13:37.
113. Knopp S., Salim N., Schindler T., Karagiannis Voules D.A., Rothen J., Lweno O., et al. Diagnostic accuracy of Kato-Katz, FLOTAC, Baermann and PCR methods for the detection of light intensity hookworm and Strongyloides stercoralis infections in Tanzania. Am J Trop Med 2014, 90:535-545.
114. Mabey D., Peeling R.W., Ustianowski A., Perkins M.D. Diagnostics for the developing world. Nat Rev Microbiol 2004, 2:231-240.
115. Bush S., Hopkins A.D. Public-private partnerships in neglected tropical disease control: the role of nongovernmental organisations. Acta Trop 2011, 120(Suppl.1):S169-S172.
116. McCarthy J.S., Lustigman S., Yang G.J., Barakat R.M., García H.H., Sripa B., et al. Aresearch agenda for helminth diseases of humans: diagnostics for control and elimination programmes. PLoS Negl Trop Dis 2012, 6:e1601.
117. Endeshaw T., Gebre T., Ngondi J., Graves P.M., Shargie E.B., Ejigsemahu Y., et al. Evaluation of light microscopy and rapid diagnostic test for the detection of malaria under operational field conditions: a household survey in Ethiopia. Malar J 2008, 7:118.
118. Yansouni C.P., Merckx J., Libman M.D., Ndao M. Recent advances in clinical parasitology diagnostics. Curr Infect Dis Rep 2014, 16:434.
119. Gordon C.A., Acosta L.P., Gobert G.N., Olveda R.M., Ross A.G., Williams G.M., et al. Real-time PCR demonstrates high prevalence of Schistosoma japonicum in the Philippines: implications for surveillance and control. PLoS Negl Trop Dis 2015, 9:e0003483.
120. Wilson A.R., van Dam G.J., Kariuki T.M., Farah I.O., Deelder A.M., Coulson P.S. The detection limits for estimates of infection intensity inschistosomiasis mansoni established by a study in non-human primates. Int J Parasitol 2006, 36:1241-1244.
121. van't Wout A.B., de Jonge N., Wood S.M., van Lieshout L., Mitchell G.F., Deelder A.M. Serum levels of circulating anodic antigen and circulating cathodic antigen detected in mice infected with Schistosoma japonicum or S.mansoni. Parasitol Res 1995, 81:434-437.
122. de Jonge N., De Caluwe P., Hilberath G.W., Krijger F.W., Polderman A.M., Deelder A.M. Circulating anodic antigen levels in serum before and after chemotherapy with praziquantel in schistosomiasis mansoni. Trans R Soc Trop Med Hyg 1989, 83:368-372.
123. Doenhoff M.J., Chiodini P.L., Hamilton J.V. Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies?. Trends Parasitol 2004, 20:35-39.
124. Kajihara N., Hirayama K. The war against a regional disease in Japan. A history of the eradication of schistosomiasis japonica. Trop Med Health 2011, 39:3-44.
125. Yang G.J., Liu L., Zhu H.R., Griffiths S.M., Tanner M., Bergquist R., et al. China's sustained drive to eliminate neglected tropical diseases. Lancet Infect Dis 2014, 14:881-892.