Skip to main content
×
×
Home

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

  • Paul Ogongo (a1) (a2), Thomas M. Kariuki (a1) (a3) and R. Alan Wilson (a4)
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.

Copyright
Corresponding author
Author for correspondence: Paul Ogongo, E-mail: polikogongo@gmail.com
References
Hide All
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), 427432.
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), 4149.
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), 5356.
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), 960966.
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), 354357.
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), 181187.
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), 13. doi: 10.1590/0102-311X00190815.
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), 681686.
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), 6066012.
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), 3151031517.
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, 352358.
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), 19361940.
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), 339345.
Braschi, S and Wilson, RA (2006) Proteins exposed at the adult schistosome surface revealed by biotinylation. Molecular Cell Proteomics 5, 347356.
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), 205212.
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, 14711482.
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, 237246.
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), 15171524.
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, 8493.
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.
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), 280286.
Chitsulo, L, Loverde, PT and Engels, D (2004) Schistosomiasis. Nature Reviews. Microbiology 2(1), 1213.
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, 426432.
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.
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, 214220.
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), 18411855.
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, 503515.
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), 835844.
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), 268272.
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), 233238.
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, 10991103. Tropical Medicine and International Health 17, 402–403.
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, 11121121.
De Vlas, SJ and Gryseels, B (1992) Underestimation of Schistosoma mansoni prevalence. Parasitology Today 8, 274277.
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), 3539.
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), 183187.
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), 721727.
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), 319324.
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), 139146.
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, 195197.
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), 591594.
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), 815818.
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), 756759.
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, 2834.
Feldmeier, H and Poggensee, G (1993) Diagnostic techniques in schistosomiasis control. A review. Acta Tropica 52(4), 205220.
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, 191198.
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.
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), 191195.
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, 865878.
Hall, J E. (2016). Guyton and Hall Textbook of Medical Physiology, 13th edn., Philadelphia, PA: Elsevier.
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), 1829.
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), 7380.
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), 907911.
Hamilton, JV, Klinkert, M and Doenhoff, MJ (1998) Diagnosis of schistosomiasis: antibody detection, with notes on parasitological and antigen detection methods. Parasitology 117(Suppl), S41S57.
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), 737744.
Hinz, R, Schwarz, NG, Hahn, A and Frickmann, H (2017) Serological approaches for the diagnosis of schistosomiasis – A review. Molecular and Cellular Probes 31, 221.
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.
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), 7384.
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, 281288.
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, 55265529, [PubMed: 15322059].
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, 39793986.
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), 325329.
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), 397400.
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), 605610.
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), 11901194.
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), 163169.
Lengeler, C, Utzinger, J and Tanner, M (2002) Screening for schistosomiasis with questionnaires. Trends in Parasitology 18(9), 375377.
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, 1418.
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), 12251234.
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), 4650.
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), 977984.
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, 338344.
Marti, H and Escher, E (1990) SAF – an alternative fixation solution for parasitological stool specimens. Schweizerische Medizinische Wochenschrift 120, 14731476.
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), 617628.
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, 29882991.
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.
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), 831840.
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), 150154.
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, 939943.
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.
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), 167169.
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), 625633.
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), 315326.
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, 255261, [in Portuguese].
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), 360366.
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, 664673.
Pellegrino, J and Coelho, PM (1978) Schistosoma mansoni: wandering capacity of a worm couple. Journal of Parasitology 64, 181182.
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.
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), 873876.
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), 152157.
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), 534537.
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), 157162.
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), 652656.
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), 303306.
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), 322328.
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), 304308.
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), 7983.
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), 18271879.
Ross, AG, Vickers, D, Olds, GR, Shah, SM and McManus, DP (2007) Katayama syndrome. The Lancet Infectious Diseases 7(3), 218224.
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.
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), 325331.
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), 8488.
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), 7380.
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.
Siddiqui, AA and Siddiqui, SZ (2017) Sm-p80-Based schistosomiasis vaccine: preparation for human clinical trials. Trends in Parasitology 33(3), 194201.
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), 640644.
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), 169180.
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.
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), 411425.
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), 575579.
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, 2028.
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), 369373.
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.
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, 358362.
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), 467482.
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), 54585461.
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, 274282.
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), 311312.
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), 519526.
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), 1929.
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), 6980.
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, 148157.
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, 213220.
Weerakoon, KGAD, Gobert, GN, Cai, P and McManus, DP (2015) Advances in the diagnosis of human schistosomiasis. Clinical Microbiology Reviews 28(4), 939967
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.
Wilson, RA (2012) Proteomics at the schistosome-mammalian host interface: any prospects for diagnostics or vaccines? Parasitology 139, 11781194.
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), 12411244.
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, 1420.
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.
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), 327331.
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), 64956501.
Zhu, YC (2005) Immunodiagnosis and its role in schistosomiasis control in China: a review. Acta Tropica 96(2–3), 130136.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed