Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-19T05:10:29.331Z Has data issue: false hasContentIssue false
  • English
  • Français

Diagnosis of schistosomiasis mansoni: an evaluation of existing methods and research towards single worm pair detection

Published online by Cambridge University Press:  06 March 2018

Paul Ogongo ,
Thomas M. Kariuki  and
R. Alan Wilson
Paul Ogongo*
Affiliation:
Department of Tropical Infectious Diseases, Institute of Primate Research, P.O Box 24481, Karen 00502 Nairobi, Kenya Africa Health Research Institute, 4013 Durban, KwaZulu Natal, South Africa
Thomas M. Kariuki
Affiliation:
Department of Tropical Infectious Diseases, Institute of Primate Research, P.O Box 24481, Karen 00502 Nairobi, Kenya The Alliance for Accelerating Excellence in Science in Africa, Africa Academy of Sciences, P.O Box 24916, Karen 00502 Nairobi, Kenya
R. Alan Wilson
Affiliation:
Biology Department, Centre for Immunology and Infection, University of York, York YO10 5DD, UK
*
Author for correspondence: Paul Ogongo, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The inadequacy of current diagnostics for the detection of low worm burdens in humans means that schistosomiasis mansoni is more widespread than previously acknowledged. With the inception of mass drug treatment programmes aimed at disease elimination and the advent of human vaccine trials, the need for more sensitive diagnostics is evident. In this review, we evaluate the merits and limitations of the principal diagnostic methods, namely detection of eggs in faeces; anti-schistosome antibodies in serum; parasite-derived proteins and glycans in serum or urine; parasite DNA in blood, faeces or urine. Only in the baboon model, where actual worm burden is determined by portal perfusion, have faecal smear and circulating antigen methods been calibrated, and shown to have thresholds of detection of 10–19 worm pairs. There is scope for improvement in all the four methods of detection, e.g. the identification of single targets for host antibodies to improve the specificity of enzyme linked immunosorbent assay. Despite recent advances in the definition of the schistosome secretome, there have been no comprehensive biomarker investigations of parasite products in the urine of infected patients. Certainly, the admirable goal of eliminating schistosomiasis will not be achieved unless individuals with low worm burdens can be diagnosed.

Keywords

Antibody ELISAbaboon modelbiomarkerscirculating antigendiagnosticsDNA detectionfaecal egg countSchistosoma mansoniworm burden
Type
Review Article
Information
Parasitology , Volume 145 , Issue 11 , September 2018 , pp. 1355 - 1366
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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

Abbasi, I, King, CH, Muchiri, EM and Hamburger, J (2010) Detection of Schistosoma mansoni and Schistosoma haematobium DNA by loop-mediated isothermal amplification: identification of infected snails from early prepatency. The American Journal of Tropical Medicine and Hygiene 83(2), 427–432.Google Scholar
Alarcón de Noya, B, Ruiz, R, Losada, S, Colmenares, C, Contreras, R, Cesari, IM and Noya, O (2007) Detection of schistosomiasis cases in low-transmission areas based on coprologic and serologic criteria: the Venezuelan experience. Acta Tropica 103(1), 41–49.Google Scholar
Alves-Brito, CF, Simpson, AJ, Bahia-Oliverira, LM, Rabello, AL, Rocha, RS, Lambertucci, JR, Gazzinelli, G, Katz, N and Correa-Oliveira, R (1992) Analysis of anti-keyhole limpet haemocyanin antibody in Brazilians supports its use for the diagnosis of acute schistosomiasis mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 86(1), 53–56.Google Scholar
Al-Sherbiny, MM, Osman, AM, Hancock, K, Deelder, AM and Tsang, VC (1999) Application of immunodiagnostic assays: detection of antibodies and circulating antigens in human schistosomiasis and correlation with clinical findings. The American Journal of Tropical Medicine and Hygiene 60(6), 960–966.Google Scholar
Attallah, AM, Ismail, H, El Masry, SA, Rizk, H, Handousa, A, El Bendary, M, Tabll, A and Ezzat, F (1999) Rapid detection of a Schistosoma mansoni circulating antigen excreted in urine of infected individuals by using a monoclonal antibody. Journal of Clinical Microbiology 37(2), 354–357.Google Scholar
Barreto, ML, Silva, JT, Mott, KE and Lehman, JS Jr (1978) Stability of faecal egg excretion in Schistosoma mansoni infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 72(2), 181–187.Google Scholar
Barreto, MS, Gomes, EC and Barbosa, CS (2016) High-risk tourism in areas vulnerable to schistosomiasis mansoni transmission in Brazil. Cadernos de Saude Publica 32(3), 1–3. doi: 10.1590/0102-311X00190815.Google Scholar
Barsoum, IS, Bogitsh, BJ and Colley, DG (1992) Detection of Schistosoma mansoni circulating cathodic antigen for evaluation of resistance induced by irradiated cercariae. The Journal of Parasitology 78(4), 681–686.Google Scholar
Berggren, WL and Weller, TH (1967) Immunoelectrophoretic demonstration of specific circulating antigen in animals infected with Schistosoma mansoni. The American Journal of Tropical Medicine and Hygiene 16(5), 606–6012.Google Scholar
Bergwerff, AA, van Dam, GJ, Rotmans, JP, Deelder, AM, Kamerling, JP and Vliegenthart, JF (1994) The immunologically reactive part of immunopurified circulating anodic antigen from Schistosoma mansoni is a threonine-linked polysaccharide consisting of --> 6)-(beta-D-GlcpA-(1 --> 3))-beta-D- GalpNAc-(1 --> repeating units. The Journal of Biological Chemistry 269(50), 31510–31517.+6)-(beta-D-GlcpA-(1+-->+3))-beta-D-+GalpNAc-(1+-->+repeating+units.+The+Journal+of+Biological+Chemistry+269(50),+31510–31517.>Google Scholar
Berriman, M, Haas, BJ, LoVerde, PT, Wilson, RA, Dillon, GP, Cerqueira, GC, Mashiyama, ST, Al-Lazikani, B, Andrade, LF, Ashton, PD, Aslett, MA, Bartholomeu, DC, Blandin, G, Caffrey, CR, Coghlan, A, Coulson, R, Day, TA, Delcher, A, DeMarco, R, Djikeng, A, Eyre, T, Gamble, JA, Ghedin, E, Gu, Y, Hertz-Fowler, C, Hirai, H, Hirai, Y, Houston, R, Ivens, A, Johnston, DA, et al. (2009) The genome of the blood fluke Schistosoma mansoni. Nature 460, 352–358.Google Scholar
Boehme, CC, Nabeta, P, Henostroza, G, Raqib, R, Rahim, Z, Gerhardt, M, Sanga, E, Hoelscher, M, Notomi, T, Hase, T and Perkins, MD (2007) Operational feasibility of using loop-mediated isothermal amplification for diagnosis of pulmonary tuberculosis in microscopy centers of developing countries. Journal of Clinical Microbiology 45(6), 1936–1940.Google Scholar
Bottieau, E, Clerinx, J, de Vega, MR, Van den Enden, E, Colebunders, R, Van Esbroeck, M, Vervoort, T, Van Gompel, A and Van den Ende, J (2006) Imported Katayama fever: clinical and biological features at presentation and during treatment. The Journal of Infection 52(5), 339–345.Google Scholar
Braschi, S and Wilson, RA (2006) Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular Cell Proteomics 5, 347–356.Google Scholar
Braschi, S, Castro-Borges, W and Wilson, RA (2006 a) Proteomic analysis of the schistosome tegument and its surface membranes. Memórias do Instituto Oswaldo Cruz 101(Suppl 1), 205–212.Google Scholar
Braschi, S, Curwen, RS, Ashton, PD, Verjovski-Almeida, S and Wilson, A (2006 b) The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction. Proteomics 6, 1471–1482.Google Scholar
Cai, P, Weerakoon, KG, Mu, Y, Olveda, DU, Piao, X, Liu, S, Olveda, RM, Chen, Q, Ross, AG and McManus, DPA (2017) Parallel comparison of antigen candidates for development of an optimized serological diagnosis of schistosomiasis japonica in the Philippines. EBioMedicine 24, 237–246.Google Scholar
Carabin, H, Balolong, E, Joseph, L, McGarvey, ST, Johansen, MV, Fernandez, T, Willingham, AL and Olveda, R (2005) Estimating sensitivity and specificity of a faecal examination method for Schistosoma japonicum infection in cats, dogs, water buffaloes, pigs, and rats in western samar and sorsogon provinces, the Philippines. International Journal for Parasitology 35(14), 1517–1524.Google Scholar
Cass, CL, Johnson, JR, Califf, LL, Xu, T, Hernandez, HJ, Stadecker, MJ, Yates, JR 3rd and Williams, DL (2007) Proteomic analysis of Schistosoma mansoni egg secretions. Molecular and Biochemical Parasitology 155, 84–93.Google Scholar
Castro-Borges, W, Dowle, A, Curwen, RS, Thomas-Oates, J and Wilson, RA (2011) Enzymatic shaving of the tegument surface of live schistosomes for proteomic analysis: a rational approach to select vaccine candidates. PLoS Neglected Tropical Diseases 5(3), e993.Google Scholar
Cesari, IM, Ballen, DE, Mendoza, L and Matos, C (2005) Detection of Schistosoma mansoni membrane antigens by immunoblot analysis of sera of patients from low-transmission areas. Clinical and Diagnostic Laboratory Immunology 12(2), 280–286.Google Scholar
Chitsulo, L, Loverde, PT and Engels, D (2004) Schistosomiasis. Nature Reviews. Microbiology 2(1), 12–13.Google Scholar
Colley, DG, Binder, S, Campbell, C, King, CH, Tchuem Tchuente, LA, N'Goran, EK, Erko, B, Karanja, DM, Kabatereine, NB, 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. The American Journal of Tropical Medicine Hygiene 88, 426–432.Google Scholar
Colley, DG, Andros, TS and Campbell, CH Jr (2017) Schistosomiasis is more prevalent than previously thought: what does it mean for public health goals, policies, strategies, guidelines and intervention programs? Infectious Diseases of Poverty 6, 63.Google Scholar
Coltart, CEM, Chew, A, Storrar, N, Armstrong, M, Suff, N, Morris, L, Chiodini, PL and Whitty, CJM (2015) Schistosomiasis presenting in travellers: a 15 year observational study at the hospital for tropical diseases, London. Transactions of the Royal Society of Tropical Medical and Hygiene 109, 214–220.Google Scholar
Corstjens, PL, De Dood, CJ, Kornelis, D, Fat, EM, Wilson, RA, Kariuki, TM, Nyakundi, RK, Loverde, PT, Abrams, WR, Tanke, HJ, Van Lieshout, L, Deelder, AM and Van Dam, GJ (2014) Tools for diagnosis, monitoring and screening of Schistosoma infections utilizing lateral-flow based assays and upconverting phosphor labels. Parasitology 141(14), 1841–1855.Google Scholar
Cringoli, G, Rinaldi, L, Maurelli, MP and 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
Curwen, RS, Ashton, PD, Sundaralingam, S and Wilson, RA (2006) Identification of novel proteases and immunomodulators in the secretions of schistosome cercariae that facilitate host entry. Molecular & Cellular Proteomics 5(5), 835–844.Google Scholar
Deelder, AM, De Jonge, N, Boerman, OC, Fillié, YE, Hilberath, GW, Rotmans, JP, Gerritse, MJ and Schut, DW (1989) Sensitive determination of circulating anodic antigen in Schistosoma mansoni infected individuals by an enzyme-linked immunosorbent assay using monoclonal antibodies. The American Journal of Tropical Medicine and Hygiene 40(3), 268–272.Google Scholar
Deelder, AM, Qian, ZL, Kremsner, PG, Acosta, L, Rabello, AL, Enyong, P, Simarro, PP, van Etten, EC, Krijger, FW and Rotmans, JP (1994) Quantitative diagnosis of schistosoma infections by measurement of circulating antigens in serum and urine. Tropical and Geographical Medicine 46(4 Spec No), 233–238.Google Scholar
Deelder, AM, van Dam, GJ, van Lieshout, L (2012) Response to: accuracy of circulating cathodic antigen tests for rapid mapping of Schistosoma mansoni and S. haematobium infections in Southern Sudan by RA Sshton et al. (2011) Tropical Medicine & International Health 16, 1099–1103. Tropical Medicine and International Health 17, 402–403.Google Scholar
DeMarco, R, Mathieson, W, Manuel, SJ, Dillon, GP, Curwen, RS, Ashton, PD, Ivens, AC, Berriman, M, Verjovski-Almeida, S and Wilson, RA (2010) Protein variation in blood-dwelling schistosome worms generated by differential splicing of micro-exon gene transcripts. Genome Research 20, 1112–1121.Google Scholar
De Vlas, SJ and Gryseels, B (1992) Underestimation of Schistosoma mansoni prevalence. Parasitology Today 8, 274–277.Google Scholar
Doenhoff, MJ, Chiodini, PL and Hamilton, JV (2004) Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies? Trends in Parasitology 20(1), 35–39.Google Scholar
Eberl, M, Al-Sherbiny, M, Hagan, P, Ljubojevic, S, Thomas, AW and Wilson, RA (2002) A novel and sensitive method to monitor helminth infections by faecal sampling. Acta Tropica 83(2), 183–187.Google Scholar
El-Sayed, LH, Ghoneim, H, Demian, SR, El-Sayed, MH, Tawfik, NM, Sakr, I, Abou-Basha, LM, Renganathan, E, Klinkert, MQ and Abou-Rawash, N (1998) Diagnostic significance of Schistosoma mansoni proteins Sm31 and Sm32 in human schistosomiasis in an endemic area in Egypt. Tropical Medicine and International Health 3(9), 721–727.Google Scholar
Engels, D, Sinzinkayo, E and Gryseels, B (1996) Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications. The American Journal of Tropical Medicine and Hygiene 54(4), 319–324.Google Scholar
Engels, D, Chitsulo, L, Montresor, A and Savioli, L (2002) The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Tropica 82(2), 139–146.Google Scholar
de Jonge, N, Fillie, YE and Deelder, AM (1987) A simple and rapid treatment (trichloroacetic-acid precipitation) of serum samples to prevent nonspecific reactions in the immunoassay of a proteoglycan. Journal of Immunological Methods 99, 195–197.Google Scholar
de Jonge, N, Gryseels, B, Hilberath, GW, Polderman, AM and Deelder, AM (1988) Detection of circulating anodic antigen by ELISA for seroepidemiology of schistosomiasis mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 82(4), 591–594.Google Scholar
de Jonge, N, Kremsner, PG, Krijger, FW, Schommer, G, Fillié, YE, Kornelis, D, van Zeyl, RJ, van Dam, GJ, Feldmeier, H and Deelder, AM (1990) Detection of the schistosome circulating cathodic antigen by enzyme immunoassay using biotinylated monoclonal antibodies. Transactions of the Royal Society of Tropical Medicine and Hygiene 84(6), 815–818.Google Scholar
De Jonge, N, Rabello, AL, Krijger, FW, Kremsner, PG, Rocha, RS, Katz, N and Deelder, AM (1991) Levels of the schistosome circulating anodic and cathodic antigens in serum of schistosomiasis patients from Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 85(6), 756–759.Google Scholar
Favero, V, Candido, RRF, Verissimo, CM, Jones, MK, St. Pierre, TG, Lindholz, CG, Da Silva, VD, Morassutti, AL and Graeff-Teixeira, C (2017) Optimization of the helmintex method for schistosomiasis diagnosis. Experimental Parasitology 177, 28–34.Google Scholar
Feldmeier, H and Poggensee, G (1993) Diagnostic techniques in schistosomiasis control. A review. Acta Tropica 52(4), 205–220.Google Scholar
Fenwick, A (2017) Schistosomiasis research and control since the retirement of Sir Patrick Manson in 1914. Transaction of the Royal Society of Tropical Medicine and Hygiene 111, 191–198.Google Scholar
Glinz, D, Silue, KD, Knopp, S, Lohourignon, LK, Yao, KP, Steinmann, P, Rinaldi, L, Cringoli, G, N'Goran, EK 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(7), e754.Google Scholar
Gonzalez, AY, Sulbaran, GS, Ballen, DE and Cesari, IM (2016) Immunocapture of circulating Schistosoma mansoni cathepsin B antigen (Sm31) by anti-Sm31 polyclonal antibodies. Parasitology International 65(3), 191–195.Google Scholar
Grzych, JM, Dissous, C, Capron, M, Torres, S, Lambert, PH and Capron, A (1987) Schistosoma mansoni shares a protective carbohydrate epitope with keyhole limpet hemocyanin. Journal of Experimental Medicine 165, 865–878.Google Scholar
Hall, J E. (2016). Guyton and Hall Textbook of Medical Physiology, 13th edn., Philadelphia, PA: Elsevier.Google Scholar
Hall, SL, Braschi, S, Truscott, M, Mathieson, W, Cesari, IM and Wilson, RA (2011) Insights into blood feeding by schistosomes from a proteomic analysis of worm vomitus. Molecular and Biochemical Parasitology 179(1), 18–29.Google Scholar
Hamburger, J, Turetski, T, Kapeller, I and Deresiewicz, R (1991) Highly repeated short DNA sequences in the genome of Schistosoma mansoni recognized by a species-specific probe. Molecular and Biochemical Parasitology 44(1), 73–80.Google Scholar
Hamburger, J, Abbasi, I, Ramzy, RM, Jourdane, J and Ruppel, A (2001) Polymerase chain reaction assay based on a highly-repeated sequence of Schistosoma haematobium: a potential tool for monitoring schistosome-infested ater. The American Journal of Tropical Medicine and Hygiene 65(6), 907–911.Google Scholar
Hamilton, JV, Klinkert, M and Doenhoff, MJ (1998) Diagnosis of schistosomiasis: antibody detection, with notes on parasitological and antigen detection methods. Parasitology 117(Suppl), S41–S57.Google Scholar
Hassan, MM, Badawi, MA and Strand, M (1992) Circulating schistosomal antigen in diagnosis and assessment of cure in individuals infected with Schistosoma mansoni. The American Journal of Tropical Medicine and Hygiene 46(6), 737–744.Google Scholar
Hinz, R, Schwarz, NG, Hahn, A and Frickmann, H (2017) Serological approaches for the diagnosis of schistosomiasis – A review. Molecular and Cellular Probes 31, 2–21.Google Scholar
Hotez, PJ and Kamath, A (2009) Neglected tropical diseases in sub-Saharan Africa: review of their prevalence, distribution, and disease burden. PLoS Neglected Tropical Diseases 3(8), e412.Google Scholar
Ishida, MMI, Rubinsky-Elefant, G, Ferreira, AW, Hoshino-Shimizu, S and Vaz, AJ (2003) Helminth antigens (Taenia solium, Taenia crassiceps, Toxocara canis, Schistosoma mansoni and Echinococcus granulosus) and cross-reactivities in human infections and immunized animals. Acta Tropica 89(1), 73–84.Google Scholar
Kariuki, TM and Farah, IO (2005) Resistance to re-infection after exposure to normal and attenuated schistosome parasites in the baboon model. Parasite Immunology 27, 281–288.Google Scholar
Kariuki, TM, Farah, IO, Yole, DS, Mwenda, JM, van Dam, GJ, Deelder, AM, Wilson, RA and Coulson, PS (2004) Parameters of the attenuated schistosome vaccine evaluated in the olive baboon. Infection and Immunity 72, 5526–5529, [PubMed: 15322059].Google Scholar
Kariuki, TM, van Dam, GJ, Deelder, AM, Farah, IO, Yole, DS, Wilson, RA and Coulson, PS (2006) Previous or ongoing schistosome infections do not compromise the efficacy of the attenuated cercaria vaccine. Infection and Immunity 74, 3979–3986.Google Scholar
Kato-Hayashi, N, Kirinoki, M, Iwamura, Y, Kanazawa, T, Kitikoon, V, Matsuda, H and Chigusa, Y (2010) Identification and differentiation of human schistosomes by polymerase chain reaction. Experimental Parasitology 124(3), 325–329.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 De São Paulo 14(6), 397–400.Google Scholar
Kittur, N, Castleman, JD, Campbell, CH Jr, King, CH and Colley, DG (2016) Comparison of Schistosoma mansoni prevalence and intensity of infection, as determined by the circulating cathodic antigen urine assay or by the Kato-Katz fecal assay: a systematic review. The American Journal of Tropical Medicine and Hygiene 94(3), 605–610.Google Scholar
Knopp, S, Glinz, D, Rinaldi, L, Mohammed, KA, N'Goran, EK, Stothard, JR, Marti, H, Cringoli, G, Rollinson, D and Utzinger, J (2009) FLOTAC: a promising technique for detecting helminth eggs in human faeces. Transactions of the Royal Society of Tropical Medicine and Hygiene 103(12), 1190–1194.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(3), 163–169.Google Scholar
Lengeler, C, Utzinger, J and Tanner, M (2002) Screening for schistosomiasis with questionnaires. Trends in Parasitology 18(9), 375–377.Google Scholar
Li, YL, Idris, MA, Corachan, M, Han, JJ, Kirschfink, M and Ruppel, A (1996) Circulating antigens in schistosomiasis: detection of 31/32 kDa proteins in sera from patient infected with Schistosoma japonicum, S. mansoni, S. haematobium, or S. intercalatum. Parasitology Research 82, 14–18.Google Scholar
Liu, S, Zhou, X, Piao, X, Hou, N, Shen, Y, Zou, Y, Li, S, Cao, J and Chen, Q (2016) Saposin-like proteins, a multigene family of Schistosoma species, are biomarkers for the immunodiagnosis of schistosomiasis japonica. Journal of Infectious Diseases 214(8), 1225–1234.Google Scholar
Lodh, N, Mwansa, JCL, Mutengo, MM and Shiff, CJ (2013) Diagnosis of Schistosoma mansoni without the stool: comparison of three diagnostic tests to detect schiostosoma mansoni infection from filtered urine in Zambia. The American Journal of Tropical Medicine Hygiene 89(1), 46–50.Google Scholar
Magalhães, RJS, Salamat, MS, Leonardo, L, Gray, DJ, Carabin, H, Halton, K, McManus, DP, Williams, GM, Rivera, P, Saniel, O, Hernandez, L, Yakob, L, McGarvey, S and Archie Clements, A (2014) Geographical distribution of human Schistosoma japonicum infection in The Philippines: tools to support disease control and further elimination. International Journal of Parasitology 44(13), 977–984.Google Scholar
Mansour, MK, Omer-Ali, P, Farid, Z, Simpson, AJG and Woody, JW (1989) Serological differentiation of acute and chronic schistosomiasis mansoni by antibody responses to keyhole limpet hemocyanin. The American Journal of Tropical Medicine 41, 338–344.Google Scholar
Marti, H and Escher, E (1990) SAF – an alternative fixation solution for parasitological stool specimens. Schweizerische Medizinische Wochenschrift 120, 1473–1476.Google Scholar
Mathieson, W and Wilson, RA (2010) A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: the miracidium, hatch fluid and secretions. International Journal of Parasitology 40(5), 617–628.Google Scholar
Merrifield, M, Hotez, PJ, Beaumier, CM, Gillespie, P, Strych, U, Hayward, T and Bottazzi, ME (2016) Advancing a vaccine to prevent human schistosomiasis. Vaccine 34, 2988–2991.Google Scholar
Meurs, L, Brienen, E, Mbow, M, Ochola, EA, Mboup, S, Karanja, DMS, Secor, WE, Polman, K and van Lieshout, L (2015) Is PCR the next reference standard for the diagnosis of schistosoma in stool? A comparison with microscopy in Senegal and Kenya. PLoS Neglected Tropical Diseases 9(7), e0003959.Google Scholar
Moore, DV and Sandground, JH (1956) The relative egg producing capacity of Schistosoma mansoni and Schistosoma japonicum. The American Journal of Tropical Medicine Hygiene 5(5), 831–840.Google Scholar
Mori, Y, Nagamine, K, Tomita, N and Notomi, T (2001) Detection of loop-mediated isothermal amplification reaction by turbidity derived from magnesium pyrophosphate formation. Biochemical and Biophysical Research Communications 289(1), 150–154.Google Scholar
Nash, TE (1978) Antibody response to a polysaccharide antigen present in the schistosome gut. I. Sensitivity and specificity. American Journal of Tropical Medicine and Hygiene 27, 939–943.Google Scholar
Notomi, T, Okayama, H, Masubuchi, H, Yonekawa, T, Watanabe, T, Amino, N and Hase, T (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Research 28(12), e63.Google Scholar
Noya, O, Alarcón de Noya, B, Losada, S, Colmenares, C, Guzmán, C, Lorenzo, MA and Bermúdez, H (2002) Laboratory diagnosis of schistosomiasis in areas of low transmission: a review of a line of research. Memórias do Instituto Oswaldo Cruz 97(Suppl. 1), 167–169.Google Scholar
Obeng, BB, Aryeetey, YA, de Dood, CJ, Amoah, AS, Larbi, IA, Deelder, AM, Yazdanbakhsh, M, Hartgers, FC, Boakye, DA, Verweij, JJ, van Dam, GJ and van Lieshout, L (2008) Application of a circulating-cathodic-antigen (CCA) strip test and real-time PCR, in comparison with microscopy, for the detection of Schistosoma haematobium in urine samples from Ghana. Annals of Tropical Medicine and Parasitology 102(7), 625–633.Google Scholar
Odogwu, S. E., Ramamurthy, N. K., Kabatereine, N. B., Kazibwe, F., Tukahebwa, E., Webster, J. P., Fenwick, A. and Stothard, J. R. (2006). Schistosoma mansoni in infants (aged <3 years) along the Ugandan shoreline of lake Victoria. Annals of Tropical Medicine and Parasitology 100(4), 315–326.Google Scholar
Oliveira, EJ, Kanamura, HY, Dias, LCS, Soares, LCB, Lima, DMC and Ciaravolho, RMC (2003) IgM-ELISA for diagnosis of schistosomiasis mansoni in low endemic areas. Cadernos de Sáude Pública 19, 255–261, [in Portuguese].Google Scholar
Oliveira, EJ, Kanamura, HY, Takei, K, Hirata, RDC, Valli, LCP, Nguyen, NY, Rodrigues, IC, Jesus, AR and Hirata, MH (2008) Synthetic peptides as an antigenic base in an ELISA for laboratory diagnosis of schistosomiasis mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 102(4), 360–366.Google Scholar
Ortu, G, Ndayishimiye, O, Clements, M, Kayugi, D, Campbell, CH, Lamine, MS, Zivieri, A, Magalhaes, RS, Binder, S, King, CH, Fenwick, A, Colley, DG and Jourdan, PM (2017) Countrywide reassessment of Schistosoma mansoni infection in Burundi using a urine-circulating cathodic antigen rapid test: informing the national control program. The American Journal Tropical Medicine Hygiene 96, 664–673.Google Scholar
Pellegrino, J and Coelho, PM (1978) Schistosoma mansoni: wandering capacity of a worm couple. Journal of Parasitology 64, 181–182.Google Scholar
Pereira, TA, Syn, WK, Amancio, FF, Cunha, PHD, Caporali, JFM, Trindade, GVM, Santos, ET, Souza, MM, Andrade, ZA, Witek, RP, Secor, WE, Pereira, FEL, Lambertucci, JR and Diehl, AM (2016) Osteopontin is upregulated in human and murine acute schistosomiasis mansoni. PLoS Neglected Tropical Diseases 10, e0005057.Google Scholar
Pinheiro, MCC, Carneiro, TR, Hanemann, ALP, de Oliveira, SM and Bezerra, FSM (2012) The combination of three faecal parasitological methods to improve the diagnosis of schistosomiasis mansoni in a low endemic setting in the state of Ceará, Brazil. Memorias Instituto do Oswaldo Cruz 107(7), 873–876.Google Scholar
Polman, K, Stelma, FF, Gryseels, B, Van Dam, GJ, Talla, I, Niang, M, Van Lieshout, L and Deelder, AM (1995) Epidemiologic application of circulating antigen detection in a recent Schistosoma mansoni focus in northern Senegal. The American Journal of Tropical Medicine and Hygiene 53(2), 152–157.Google Scholar
Polman, K, Diakhate, MM, Engels, D, Nahimana, S, Van Dam, GJ, Ferreira, STMF, Deelder, AM and Gryseels, B (2000) Specificity of circulating antigen detection for schistosomiasis mansoni in Senegal and Burundi. Tropical Medicine and International Health 5(8), 534–537.Google Scholar
Pontes, LA, Dias-Neto, E and Rabello, A (2002) Detection by polymerase chain reaction of Schistosoma mansoni DNA in human serum and feces. The American Journal of Tropical Medicine and Hygiene 66(2), 157–162.Google Scholar
Pontes, LA, Oliveira, MC, Katz, N, Dias-Neto, E and Rabello, A (2003) Comparison of a polymerase chain reaction and the Kato-Katz technique for diagnosing infection with Schistosoma mansoni. The American Journal of Tropical Medicine and Hygiene 68(6), 652–656.Google Scholar
Poon, LLM, Wong, BWY, Ma, EH, Chan, KH, Chow, LMC, Abeyewickreme, W, Tangpukdee, N, Yuen, KY, Guan, Y, Looareesuwan, S and Peiris, JS (2006) Sensitive and inexpensive molecular test for falciparum malaria: detecting Plasmodium falciparum DNA directly from heat-treated blood by loop-mediated isothermal amplification. Clinical Chemistry 52(2), 303–306.Google Scholar
Rabarijaona, LP, Boisier, P, Ravaoalimalala, VE, Jeanne, I, Roux, JF, Jutand, MA and Salamon, R (2003) Lot quality assurance sampling for screening communities hyperendemic for Schistosoma mansoni. Tropical Medicine & International Health 8(4), 322–328.Google Scholar
Rabello, AL, Garcia, MM, da Silva, RAP, Rocha, RS and Katz, N (1997) Humoral immune responses in patients with acute Schistosoma mansoni infection who were followed up for two years after treatment. Clinical Infectious Diseases 24(3), 304–308.Google Scholar
Robijn, MLM, Planken, J, Dieuwke, K, Hokke, CH and Deelder, AM (2008) Mass spectrometric detection of urinary oligosaccharides as markers of Schistosoma mansoni infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 102(1), 79–83.Google Scholar
Rose, C, Parker, A, Jefferson, B and Cartmell, E (2015) The characterization of feces and urine: a review of the literature to inform advanced treatment technology. Critical Reviews in Environmental Science and Technology 45(17), 1827–1879.Google Scholar
Ross, AG, Vickers, D, Olds, GR, Shah, SM and McManus, DP (2007) Katayama syndrome. The Lancet Infectious Diseases 7(3), 218–224.Google Scholar
Rujeni, N, Morana, D, Ruberanziza, E and Mazigo, DH (2017) Schistosomiasis and soil-transmitted helminthiasis in Rwanda: an update on their epidemiology and control. Infectious Diseases of Poverty 6, 8.Google Scholar
Ruppel, A, Xing, Y, Dell, R, Numrich, P and Shi, YE (1991) Schistosoma mansoni and S. japonicum: decline of antibodies against diagnostic adult worm antigens (Sm31/32) following praziquantel treatment of mice. Tropical Medicine and Parasitology 42(4), 325–331.Google Scholar
Sandoval, N, Siles-Lucas, M, Aban, JL, Pérez-Arellano, JL, Gárate, T and Muro, A (2006) Schistosoma mansoni: a diagnostic approach to detect acute schistosomiasis infection in a murine model by PCR. Experimental Parasitology 114(2), 84–88.Google Scholar
Sauma, SY, Tanaka, TM and Strand, M (1991) Selective release of a glycosylphosphatidylinositol-anchored antigen from the surface of Schistosoma mansoni. Molecular and Biochemical Parasitology 46(1), 73–80.Google Scholar
Shane, HL, Verani, JR, Abudho, B, Montgomery, SP, Blackstock, AN, Mwinzi, PNM, Butler, SE, Karanja, DMS and Secor, WE (2011) Evaluation of urine CCA assays for detection of Schistosoma mansoni infection in Western Kenya. PLoS Neglected Tropical Diseases 5(1), e951.Google Scholar
Siddiqui, AA and Siddiqui, SZ (2017) Sm-p80-Based schistosomiasis vaccine: preparation for human clinical trials. Trends in Parasitology 33(3), 194–201.Google Scholar
Sohni, Y, Kanjilal, S and Kapur, V (2008) Performance evaluation of five commercial real-time PCR reagent systems using TaqMan assays for B. anthracis detection. Clinical Biochemistry 41(7–8), 640–644.Google Scholar
Sorgho, H, Bahgat, M, Poda, JN, Song, W, Kirsten, C, Doenhoff, MJ, Zongo, I, Ouédraogo, JB and Ruppel, A (2005) Serodiagnosis of Schistosoma mansoni infections in an endemic area of Burkina Faso: performance of several immunological tests with different parasite antigens. Acta Tropica 93(2), 169–180.Google Scholar
Sprong, H, Suchanek, M, van Dijk, SM, van Remoortere, A, Klumperman, J, Avram, D, van der Linden, J, Leusen, JH, van Hellemond, JJ and Thiele, C (2006) Aberrant receptor-mediated endocytosis of Schistosoma mansoni glycoproteins on host lipoproteins. PLoS Medicine 3, e253.Google Scholar
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. The Lancet Infectious Diseases 6(7), 411–425.Google Scholar
Stelma, FF, Talla, I, Verle, P, Niang, M and Gryseels, B (1994) Morbidity due to heavy Schistosoma mansoni infections in a recently established focus in northern Senegal. The American Journal of Tropical Medicine and Hygiene 50(5), 575–579.Google Scholar
Sulbarán, GS, Ballen, DE, Bermùdez, H, Lorenzo, M, Noya, O and Cesari, IM (2010)) Detection of the Sm31 antigen in sera ofSchistosoma mansoni- infected patients from a low endemic area. Parasite Immunology 32, 20–28.Google Scholar
Teesdale, CH, Fahringer, K and Chitsulo, L (1985) Egg count variability and sensitivity of a thin smear technique for the diagnosis of Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 79(3), 369–373.Google Scholar
Teixeira, CF, Neuhauss, E, Ben, R, Romanzini, J and Graeff-Teixeira, C (2007) Detection of Schistosoma mansoni eggs in feces through their interaction with paramagnetic beads in a magnetic field. PLoS Neglected Tropical Diseases 1(2), e73.Google Scholar
Valli, LCP, Kanamura, HY, Silva, RM, Silva, MIPG, Vellosa, SAG and Garcia, ET (1997) Efficacy of an enzyme-linked immunosorbent assay in the diagnosis of and serologic distinction between acute and chronic Schistosoma mansoni infection. The American Journal of Tropical Medicine and Hygiene 53, 358–362.Google Scholar
van Dam, GJ, Bergwerff, AA, Thomas-Oates, JE, Rotmans, JP, Kamerling, JP, Vliegenthart, JF and Deelder, AM (1994) The immunological reactive O-linked polysaccharide chains derived from circulating cathodic antigen isolated from the human blood fluke Schistosoma mansoni have lewisx as repeating unit. European Journal of Biochemistry 225(1), 467–482.Google Scholar
van Dam, GJ, Wichers, JH, Ferreira, TMF, Ghati, D, van Amerongen, A and Deelder, AM (2004) Diagnosis of schistosomiasis by reagent strip test for detection of circulating cathodic antigen. Journal of Clinical Microbiology 42(12), 5458–5461.Google Scholar
van Dam, GJ, de Dood, CJ, Lewis, M, Deelder, AM, van Lieshout, L, Tanke, HJ, van Rooyen, LH and Corstjens, PL (2013) A robust dry reagent lateral flow assay for diagnosis of active schistosomiasis by detection of Schistosoma circulating anodic antigen. Experimental Parasitology 135, 274–282.Google Scholar
van Lieshout, L, De Jonge, N, Mansour, MM, Bassily, S, Krijger, FW and Deelder, AM (1993) Circulating cathodic antigen levels in serum and urine of schistosomiasis patients before and after chemotherapy with praziquantel. Transactions of the Royal Society of Tropical Medicine and Hygiene 87(3), 311–312.Google Scholar
van Lieshout, L, de Jonge, N, El-Masry, N, Mansour, MM, Bassily, S, Krijger, FW and Deelder, AM (1994) Monitoring the efficacy of different doses of praziquantel by quantification of circulating antigens in serum and urine of schistosomiasis patients. Parasitology 108(Pt 5), 519–526.Google Scholar
van Lieshout, L, Panday, UG, De Jonge, N, Krijger, FW, Oostburg, BF, Polderman, AM and Deelder, AM (1995) Immunodiagnosis of schistosomiasis mansoni in a low endemic area in surinam by determination of the circulating antigens CAA and CCA. Acta Tropica 59(1), 19–29.Google Scholar
van Lieshout, L, Polderman, AM and Deelder, AM (2000) Immunodiagnosis of schistosomiasis by determination of the circulating antigens CAA and CCA, in particular in individuals with recent or light infections. Acta Tropica 77(1), 69–80.Google Scholar
Verjovski-Almeida, S, DeMarco, R, Martins, EA, Guimaraes, PE, Ojopi, EP, Paquola, AC, Piazza, JP, Nishiyama, MY Jr, Kitajima, JP, Adamson, RE, Ashton, PD, Bonaldo, MF, Coulson, PS, Dillon, GP, Farias, LP, Gregorio, SP, Ho, PL, Leite, RA, Malaquias, LC, Marques, RC, Miyasato, PA, Nascimento, AL, Ohlweiler, FP, Reis, EM, Ribeiro, MA, Sa, RG, Stukart, GC, Soares, MB, Gargioni, C, Kawano, T, et al. (2003) Transcriptome analysis of the acoelomate human parasite Schistosoma mansoni. Nature Genetics 35, 148–157.Google Scholar
Wasser, SK, Monfort, SL, Southers, J and Wildt, DE (1994) Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus) faeces. Journal of Reproduction and Fertility 101, 213–220.Google Scholar
Weerakoon, KGAD, Gobert, GN, Cai, P and McManus, DP (2015) Advances in the diagnosis of human schistosomiasis. Clinical Microbiology Reviews 28(4), 939–967Google Scholar
Wichmann, D, Panning, M, Quack, T, Kramme, S, Burchard, GD, Grevelding, C and Drosten, C (2009) Diagnosing schistosomiasis by detection of cell-free parasite DNA in human plasma. PLoS Neglected Tropical Diseases 3(4), e422.Google Scholar
Wilson, RA (2012) Proteomics at the schistosome-mammalian host interface: any prospects for diagnostics or vaccines? Parasitology 139, 1178–1194.Google Scholar
Wilson, RA, van Dam, GJ, Kariuki, TM, Farah, IO, Deelder, AM and Coulson, PS (2006) The detection limits for estimates of infection intensity in schistosomiasis mansoni established by a study in non-human primates. International Journal for Parasitology 36(12), 1241–1244.Google Scholar
Wilson, RA, Ashton, PD, Braschi, S, Dillon, GP, Berriman, M and Ivens, A (2007) Oming in on schistosomes: prospects and limitations for post-genomics. Trends in Parasitology 23, 14–20.Google Scholar
Wilson, RA, Li, XH, MacDonald, S, Neves, LX, Vitoriano-Souza, J, Leite, LCC, Farias, LP, James, S, Ashton, PD, DeMarco, R and Castro-Borges, W (2015) The schistosome esophagus is a ‘hotspot’ for microexon and lysosomal hydrolase gene expression: implications for blood processing. PLoS Neglected Tropical Diseases 9(12), e0004272.Google Scholar
Xu, J, Rong, R, Zhang, HQ, Shi, CJ, Zhu, XQ and Xia, CM (2010) Sensitive and rapid detection of Schistosoma japonicum DNA by loop-mediated isothermal amplification (LAMP). International Journal for Parasitology 40(3), 327–331.Google Scholar
Zhang, G, Brown, WE and González-Escalona, N (2011)) Comparison of real-time PCR, reverse transcriptase real-time PCR, loop-mediated isothermal amplification, and the FDA conventional microbiological method for the detection of S almonella spp. in produce. Applied and Environmental Microbiology 77(18), 6495–6501.Google Scholar
Zhu, YC (2005) Immunodiagnosis and its role in schistosomiasis control in China: a review. Acta Tropica 96(2–3), 130–136.Google Scholar
Zoni, AC, Catalá, L and Ault, SK (2016) Schistosomiasis prevalence and intensity of infection in Latin America and the Caribbean countries, 1942–2014: a systematic review in the context of a regional elimination goal. PLoS Neglected Tropical Diseases 10(3), e0004493.Google Scholar